Psychophysiology,32(1995),301­318.CambridgeUniversityPress.PrintedintheUSA.Orientinginadefensiveworld:Mammalianmodificationsofourevolutionaryheritage.APolyvagalTheorySTEPHENW.PORGESDepartmentofHumanDevelopment,UniversityofMaryland,CollegePark,USACopyright,1995SocietyforPsychophysiologicalResearchPRESIDENTIALADDRESS,1994AbstractThevagus,the10thcranialnerve,containspathwaysthatcontributetotheregulationoftheinternalviscera,includingtheheart.Vagalefferentfibersdonotoriginateinacommonbrainstemstructure.ThePolyvagalTheoryisintroducedtoexplainthedifferentfunctionsofthetwoprimarymedullarysourcenucleiofthevague:thenucleusambiguus(NA)andthedorsalmotornucleus(DMNX).Althoughvagalpathwaysfrombothnucleiterminateonthesinoatrialnode,itisarguedthatthefibersoriginatinginNAareuniquelyresponsibleforrespiratorysinusarrhythmia(RSA).DivergentshiftsinRSAandheartrateareexplainedbyindependentactionsofDMNXandNA.Thetheoryemphasizesaphylogeneticperspectiveandspeculatesthatmammalian,butnotreptilian,brainstemorganizationischaracterizedbyaventralvagalcomplex(includingNA)relatedtoprocessesassociatedwithattention,motion,emotion,andcommunication.Variousclinicaldisorders,suchassuddeninfantdeathsyndromeandasthma,mayberelatedtothecompetitionbetweenDMNXandNA.Descriptors:Vagus,Vagaltone,Nucleusambiguus,Dorsalmotornucleusofthevagus,Respiratorysinusarrhythmia,PolyvagalTheoryContents:

I. IntroductionII. ThePolyvagalTheory:OverviewIII. SummaryandConclusionsIV. References,AuthorNotes,andAppendicesV. Figures1–5

IntroductionThesystematicinvestigationofmind‐bodyrelationsformsthescientificbasisforthescienceofpsycho‐physiology.Unlikethecorrelativeviewofmind‐bodyevaluationsthatdominatespsychologyandpsychiatry,psychophysiologyemphasizesacontinuitybetweenneuro‐physiologicalandpsychologicalprocessing.Psycho‐physiologistsassumethatthenervoussystemprovidesthefunctionalunitsforthebidirectionaltransductionofpsychologicalandphysiologicalprocesses.Thus,fromapsychophysiologicalperspective,itispossibletolink,notmerelyintheory,butalsoviameasurement,psychologicalprocesseswithneurophysiologicalprocessesandbrainstructures.Thepaperwillfocusontheneuralregulationoftheheartviathevagusandhowthisregulationevolvedtofacilitatespecificpsychologicalprocesses.ThePoly‐VagalTheory,describedinthispaper,providesanexplanationofhowthevagalpathwaysregulateheartrateinresponsetonoveltyandtoavarietyofstressors.Thetheoryproposesthatviaevolution,mammaliannervoussystemsdevelopedtwovagalsystems:oneaphylogeneticrelicofamphibiaandreptilia,andtheother,anevolutionarymodificationuniquetomammals.AccordingtothePoly‐VagalTheory,thetwovagalsystemsareprogrammedwithdifferentresponsestrategiesandmayrespondinacontradictorymanner.Explanationsforseveralpsychophysiologicalphenomenaandpsychosomaticdisturbanceswillbeproposed.Thetheoryisbaseduponanestablishedliteratureinneurophysiology,neuroanatomy,andpsychophysiology.Arousaltheory:Historicallegacy.Earlypsychophysiologicalresearchassumedthatperipheralautonomicmeasuresprovidedsensitiveindicatorsofarousaloractivation(Darrow,Jost,Solomon,&Mergener,1942;Duffy,1957;Lindsley,1951;Malmo,1959).Thisviewwasbaseduponarudimentaryunderstandingoftheautonomicnervoussysteminwhichchangesinelectrodermalactivityandheartratewereassumedtobeaccurateindicatorsofsympatheticactivity.Asactivation‐arousaltheorydeveloped,continuitybetweentheperipheralautonomicresponseandcentralmechanismswasassumed.Accordingtothisassumption,anyorganinfluencedbysympatheticefferentfibers,suchasthesudomotor,vascular,orcardiacsystems,wasapotentialindicatoroflimbicorcorticalactivity.Althoughthespecificpathwaysrelatingthesevariouslevelswereneveroutlinedandarestillsketchy,electrodermalandheartratemeasuresbecametheprimaryfocusofresearchduringtheearlyhistoryoftheSocietyforPsychophysiologicalResearch.Thiswasduetotheirpresumedsympatheticinnervationand,inpart,totheirmeasurementavailability.Notbyplan,butbydefault,thisemphasiscreatedaresearchenvironmentthatneglectedseveralimportantfactorsincluding:1)parasympatheticinfluences,2)interactionsbetweensympatheticand

parasympatheticprocesses,3)peripheralautonomicafferents,4)centralregulatorystructures,5)theadaptiveanddynamicnatureoftheautonomicnervoussystem,and6)phylogeneticandontogeneticdifferencesinstructuralorganizationandfunction.Neglectoftheseconceptsandanemphasisonaglobalconstructof'arousal'stillabideswithinvarioussub‐disciplinesofpsychology,psychiatry,andphysiology.Thisoutdatedviewof'arousal'mayrestrictanunderstandingofhowtheautonomicnervoussysteminterfaceswiththeenvironmentandthecontributionoftheautonomicnervoussystemtopsychologicalandbehavioralprocesses.Incontrast,morerecentneurophysiologicaldatapromoteamoreintegrativeviewoftheautonomicnervoussystem.Brain­heartcommunication:Historicalperspective.Whenweviewlivingorganismsasacollectionofdynamic,adaptive,interactive,andinterdependentphysiologicalsystems,itisnolongerappropriatetotreattheautonomicnervoussystemasfunctionallydistinctfromthecentralnervoussystem.Westarttorecognizethatperipheralorgansdonot"floatinavisceralsea."Rather,theyareanchoredtocentralstructuresviaefferentpathwaysandarecontinuouslysignalingcentralregulatorystructuresviatheirabundantafferentpathways.Thus,thebidirectionalconnectionsbetweenautonomicandcentralbrainstructuresarebecomingapparent.Accordingly,newtheoriesandresearchstrategiesmustincorporatethedynamicandinteractiveconstructsthatlinkcentralstructureswithperipheralorgans.Darwin(1872)provideshistoricalinsightintothepotentialimportanceofthevagusinbidirectionalcommunicationbetweenthebrainandtheheart.AlthoughDarwinfocusedonfacialexpressionsindefiningemotions,heacknowledgedthedynamicrelationshipbetweenthevagusandthecentralnervoussystemactivitythataccompaniedthespontaneousexpressionofemotions.Hespeculatedthattherewereidentifiableneuralpathwaysthatprovidedthenecessarycommunicationbetweenspecificbrainstructuresandperipheralorganstopromotetheuniquepatternofautonomicactivityassociatedwithemotions.Forexamplehestated:...whenthemindisstronglyexcited,wemightexpectthatitwouldinstantlyaffectinadirectmannertheheart;andthisisuniversallyacknowledged...whentheheartisaffecteditreactsonthebrain;andthestateofthebrainagainreactsthroughthepneumo‐gastric[vagus]nerveontheheart;sothatunderanyexcitementtherewillbemuchmutualactionandreactionbetweenthese,thetwomostimportantorgansofthebody(p.69).ForDarwin,whenanemotionalstateoccurred,thebeatingoftheheartchangedinstantly,thechangeincardiacactivityinfluencedbrainactivity,andthebrainstemstructuresviathecranialnerves(i.e.,vagus)stimulatedtheheart.Hedidnotelucidatetheneurophysiologicalmechanismsthattranslatetheinitialemotional

expressiontotheheart.OurcurrentknowledgeofthebrainstemoriginandneurophysiologicalfunctionofthevariousbranchesofthevaguswasnotavailabletoDarwin.Atthattimeitwasnotknownthatvagalfibersoriginatedinseveralmedullarynucleiandthatthebranchesofthevagusexertedcontrolovertheperipherythroughdifferentfeedbacksystems.However,Darwin'sstatementisimportant,becauseitemphasizestheafferentfeedbackfromthehearttothebrain,independentofthespinalcordandthesympatheticnervoussystem,aswellastheregulatoryroleofthepneumo‐gastricnerve(renamedthevagusattheendofthe19thcentury)intheexpressionofemotions.DarwinattributedtheaboveideastoClaudeBernardasanexampleofnervoussystemregulationoflemilieuinterieur.Consistentwithmorecontemporarypsychophysiology,ClaudeBernardviewedtheheartasaprimaryresponsesystemcapableofrespondingtoallformsofsensorystimulation.Heexplicitlyemphasizedthepotencyofcentralnervoussystempathwaystotheheart(Cournand,1979).Theseideasareexpressedinthefollowingquotation:Inmantheheartisnotonlythecentralorganofcirculationofblood,itisacenterinfluencedbyallsensoryinfluences.Theymaybetransmittedfromtheperipherythroughthespinalcord,fromtheorgansthroughthesympatheticnervoussystem,orfromthecentralnervoussystemitself.Infactthesensorystimulicomingfromthebrainexhibittheirstrongesteffectsontheheart(ClaudeBernard,1865quotedinCournand,1979).Althoughseldomacknowledgedasfoundersofmodernpsychophysiology,BernardandDarwinhavecontributedtothetheoreticalbasisforaneuro‐psychophysiologyoftheautonomicnervoussystem.Theabovequotationsdocumenttheirviewthattheheartprovidednotonlyanoutputsystemfromthebrain,capableofindexingsensoryprocessing,buttheyalsorecognizedthattheheartwasasourceofafferentstimulationtothebrainabletochangeorcontributetopsychologicalstate.Consistentwiththistheoreticalbias,psychophysiologistsduringthepastcenturyhaveinvestigatedthefunctionalsensitivityofheartratemeasurestosensoryandaffectivestimuli(e.g.,Darrow,1929;Graham&Clifton,1966;Lacey,1967),andthedynamicfeedbackbetweenthebrainandtheheartinregulatingbothpsychologicalstateandthethresholdforsensorystimuli(e.g.,LaceyandLacey,1978).ContemporarypsychophysiologygainedmuchofitscurrenttheoreticalperspectivefromintriguingideasregardingtheinteractionbetweenautonomicandsensoryprocessesintroducedbySokolov(1963).TheSokolovianmodelcontainedalltherequisitecomponentsofanintegrativetheoryrelatingautonomicfunctiontopsychologicalstate.Themodelincluded:1)acknow‐ledgmentofbothafferentsandefferentsinbothautonomicandsomaticsystems,2)anautonomicfeedbackloop(i.e.,autonomictuning)toregulatesensorythresholds,3)aninterfacebetweenautonomicprocessesandpsychologicalphenomena(i.e.,orientinganddefensivereflexes),and,4)brainregulationofautonomicreactivityviahabituation.

TheSokolovianmodelincludedbidirectionalcommunicationbetweenbrainandperiphery.IntheSokolovian,modelautonomicprocessescontributedtothetuningofreceptorsystemstoengageordisengagewiththeexternalenvironment.ConsistentwiththeSokolovview,theLaceys(e.g.,Lacey,1967;LaceyandLacey,1978)emphasizedthebidirectionalcommunicationbetweentheafferentsinthecardiovascularsystemandbrainintheregulationofbothcardiacfunctionandsensorythreshold.Incontrast,tothisemphasisonbidirectionalcommunication,Obrist(1976)focusedonthegeneralconcordancebetweenmetabolicdemandsandheartrate.Bothargumentshavemerit.Forexample,afferentstimulationofthebaroreceptorshasimmediateeffectsonbothperipheralcardiovascularfunctionandoncentralarousalstate(Gellhorn,1964),andthemetabolicdemandsassociatedwithexercisehavedeterministicinfluences,viavagalwithdrawal,onheartrate(Obrist,1981;Rowell,1993).Heartrateresponses:AneurogenicemphasisThroughoutthehistoryoftheSocietyforPsychophysiologicalResearch,psychophysiologistshavebeenstudyingrobustphenomena,suchastheautonomiccomponentsoftheorientingreflex,oftenwithoutexplanatoryneurophysiologicalmodels.Thispaperisinresponsetothisneed.Thepaperwillprovideatheoreticalmodelbasedupontheevolutionofneuralstructuresandtheneuralregulationofautonomicprocessestoexplainseveralpsychophysiologicalphenomenaincludingorientation,attention,andemotion.Theorientingreflexprovidesanexcellentpointofembarkation.BasedupontheconvergenttheoreticalapproachesofSokolov(1963),Lacey(1967),andGrahamandClifton(1966),theorientingreflexisassumedtohaveacardiaccomponent.Thiscomponentischaracterizedbyaheartratedecelerationthatfunctionallyinfluencesperceptualthresholds,facilitatingtheprocessingofinformationregardingthestateoftheexternalenvironment.However,whataretheneuralmechanismsmediatingthecardiacorientingresponse?Or,asObrist(1976)argued,istheheartratedecelerationmerelyanepiphenomenonassociatedwithdecreasedmetabolicdemandsaccompanyingthereducedmotoractivitythatdefinesorientingandattendingbehaviors?Thetimecourseoftheresponse,theeffectsofneuralblockades,andstudieswithclinicalpopulationssupportthecontentionthatthecardiacorientingresponseisneurogenic.First,heartratedecelerationassociatedwiththecardiacorientingresponseisrapid,occurringwithinafewsecondsandusuallyreturnsrapidlytobaseline.Second,thelatencycharacteristicsofthecardiacorientingresponsearesimilartootherneurogenicbradycardicreflexessuchasopto‐vagal,vaso‐vagal,baroreceptor‐vagalandchemoreceptor‐vagalreflexes.Blockadestudieswithatropinedemonstratethatshortlatencybradycardiaassociatedwithbothorientingreflexesandclassicalconditioningaremediatedbycholinergicpathwaysviathevagus(e.g.,Berntson,Cacioppo,&Quigley,1994;Obrist,1981;Schneiderman,1974).Studieswiththeagedandotherclinicalpopulationswithperipheralneuropathiesorautonomicregulatoryproblems(e.g.,

diabetes)documentdeficitsinvagalfunction(DeMeersman,1993;Gribben,Pickering,Sleight,&Peto,1971;Weiling,vanBrederode,deRijk,Borst,&Dunning,1982;Weise&Heydenreich,1991).Additionally,studiesofindividualswithunilateralbraindamagedemonstratethatheartrateresponsesarediminishedmoreinindividualswithrightsidedamage(Yokoyama,Jennings,Ackles,Hood,&Boller,1987).Thislatterfindingisconsistentwiththeevidencethatneurophysiologicalregulationofheartrateisprimarilyviatherightvagustothesino‐atrialnode,andthatheartrateisundercontrolofhigheripsilateralstructuresinthebrain(Warwick&Williams,1975).Vagalinfluencesproducingheartratedecelerationinresponsetomildstressmayinteractsynergisticallywithsympatheticwithdrawal(Buwalda,Koolhaas&Bohus,1992).Moreover,inconditionsofanticipationofaversivestimuli,therehavebeenreportsthatheartratedecelerationis,inpart,duetosympatheticwithdrawal(Rau,1991).Althoughtherearereportsofasympatheticcontributiontostimulusdependentheartratedecelerationsshortlatencydecelerationsaredeterminedprimarilybythevagus.Thus,itmaybeargued,thatsinceshortlatencyheartratereactivityismediatedbythevagus,themagnitudeofthecardiacorientingresponseisanindexofvagalregulation.TheVagalParadoxInattemptingtostructureaneurogenicmodelofvagalregulationtoexplainpsychophysiologicalphenomena,thereisanobviousinconsistencybetweendataandtheory.Physiologicaltheoryattributesboththechronotropiccontroloftheheart(i.e.,heartrate)andtheamplitudeofrespiratorysinusarrhythmia(RSA)todirectvagalmechanisms(e.g.,Jordan,Khalid,Schneiderman&Spyer,1982;Katona&Jih,1975).However,whiletherearesituationsinwhichbothmeasurescovary(e.g.,duringexerciseandcholinergicblockade),thereareothersituationsinwhichthemeasuresappeartoreflectindependentsourcesofneuralcontrol.Severalargumentshavebeenmadetoexplainthisdiscrepancy.First,ithasbeenarguedthatRSAandaverageheartrate(duringsympatheticblockade)reflectdifferentdimensionsofvagalactivity.Forexample,averageheartratemightbeviewedasreflectingtonicvagalinfluencesandRSAasreflectingphasicvagalinfluences(e.g.,Berntson,Cacioppo,&Quigley,1993;Jennings&McKnight,1994;Malik&Camm,1993).Second,ithasbeenarguedthatthediscrepancyiscausedbyvariationsinrespiratoryparameters(Grossman,Karemaker,&Wieling,1991)withRSAbeingconfoundedbyrespiratoryfrequencyandtidalvolume.Third,ithasbeenarguedthatvariationinquantificationmethodsmaycontributetothedivergencebetweenRSAandheartrate(Porges&Bohrer,1990;Byrne&Porges,1993).Andfourth,ithasbeenarguedthataverageheartrateisinfluencedbyacomplexanddynamicinteractionbetweensympatheticandvagalsystemsmakingitdifficulttoextractavagaltonedimension(Berntson,Cacioppo,andQuigley,1991,1993).

Often,theargumentshavebeenlinkedtoadefinitionofvagaltonedeterminedvianeuralblockade.Thefunctionaleffectoftheneuralblockadeonheartratehasbeenusedasthecriterionmeasureofvagaltoneorparasympatheticcontrol(e.g.,Katona&Jih,1975).ResearchershavearguedthatRSAisnotanaccurateindexofvagaltone,becauseindividualpre‐blockadelevelsofRSAdonotaccuratelymapintopre‐postchangeinheartrate(Grossman&Kollai,1993).Contrarytothisargument,Porges(1986)arguedthatthediscrepancywas,inpart,baseduponthecriterionmeasureselected.HedemonstratedthatRSAexhibitedamoresensitivedose‐dependentresponsecurvetovagalblockadeviaatropinethanheartrate.ThissuggeststhepossibilitythatRSA,monitoredduringperiodsofspontaneousbreathing,mayprovideabettercriterionvariablethanheartrate.Neurophysiologicalsupportmaybeofferedforthisproposal.RSAisavagalphenomenonincontrasttoheartrate,whichisdeterminedbyseveralsourcesincludingvagal,sympathetic,andmechanicalfactors.Thus,theefficacyofchangeinheartratefollowingcholinergicblockadeasanindexofvagaltonemaybechallenged.TheaboveargumentshavecreatedavolatileenvironmentdebatingtheneurophysiologicalinterpretationofRSAandtheefficacyofspecificmethodstoquantifyingRSA.Commontotheseargumentsistheassumptionthatthereisonecentralsourceofcardiacvagaltone.Theargumentsattributedifferences,nottocentralmechanisms,buttotheresponsecharacteristicsofheartrateandRSA.Thus,divergencehasbeenattributedtoeitherthetransferfunctionofthesino‐atrialnodethatwouldattenuatehighfrequencyoscillations(Saul,Berger,Chen,&Cohen,1989)orthestatisticaltransferfunctionofthemethodofquantifyingRSA(Byrne&Porges,1993)andnotasafunctionofdifferentialneuraloutput.However,independentofthequantificationmethodologyandduringperiodsofstablerespiratoryparameters,datahaveaccumulatedthatdemonstratethatRSAandheartrate(independentofsympatheticinfluences)oftenresponddifferently.AlthoughboththeneurogenicbradycardiaandthesuppressionofRSAorheartratevariabilityobservedduringattentionareassumedtobevagalinorigin,theyoftenappearindependentofeachotherorinanapparentphysiologicalcontradiction(Porges&Raskin,1969;Porges,1972;Richards&Casey,1991).SimilardisparitiesbetweenlevelsofheartrateandRSAhavebeenobservedduringinhalantanesthesiawhenRSAexhibitsamassivedepression,whileheartrateisnotaltered(Donchin,Feld,&Porges,1985).AdditionalexamplesofconvergenceanddivergencebetweenRSAandheartratecanbeobservedinbothwithin‐andbetween‐subjectsdesigns.Forexample,individualdifferencesinheartrateandRSAmonitoredduringrestingconditionsprovideindependentcontributionstomeasuresofcardiacvagaltonederivedfromvagalblockade(e.g.,Grossman&Kollai,1993).However,convergencemaybeobservedwithinanindividualduringexercisewhenmonotonicincreasesinmetabolicloadarereflectedinbothfasterheartrateandlowerRSA(Billman&DuJardin,1990).Or,convergencecanbeobservedduringneuralblockade,viaatropine,whenbothcardiacindicesdiminishinacleardoseresponsemanner

(Cacioppo,Berntson,Binkley,Quigley,Uchino,&Fieldstone,1994;Dellinger,Taylor,&Porges,1987;Porges,1986).TherelationshipbetweenRSAandheartratemaychangewithinandbetweenindividuals.InourlaboratorywehaveobservedthattherelationshipbetweenRSAandheartratevarieswithbehavioralstate(Riniolo,Doussard‐Roosevelt,&Porges,1994).Twenty‐four‐hourambulatorymonitoringofadultsindicatesthatduringstatesofdrowsinessandsleepthecorrelationbetweenRSAandheartrateissignificantlylowerthanduringalertstates.Thus,attimes,RSAandheartrateappeartoreflectthesamephysiologicalprocesses,whileatothertimestheyappeartoreflectindependentprocesses.Incontrasttotheobservabledata,neuro‐physiologicalresearcharguesforacovariationbetweenthesetwoparameters,becausevagalcardioinhibitoryfiberstothehearthaveconsistentfunctionalpropertiescharacterizedbybradycardiatoneuralstimulationandarespiratoryrhythm(e.g.,Jordan,Khalid,Schneiderman,&Spyer,1982).Thisinconsistency,baseduponanassumptionofasinglecentralvagalsourceislabeledtheVagalParadoxandisoutlinedinTable1.Table1TheVagalParadox:Acommoncentralsource?

1.Increasedvagaltoneproducesneurogenicbradycardia2.DecreasedvagaltoneproducessuppressionofRSA.3.BradycardiaoccurduringperiodsofsuppressedRSA.

TheVagalParadoxiscriticaltotheinterpretationofseveralpsychophysiologicalandclinicalconditions.Forexample,ifthebradycardiaoccurringduringorientingreflexesarevagal,whyarebradycardiaoftenobservedduringperiodsofreducedRSA,alsoanindexofbothattentionandvagalcontroloftheheart?IfvagaltoneisapositiveindicatorofhealthofafetusorneonatewhenmonitoredwithRSA,whyisvagaltoneanegativeindicatorofhealthwhenitismanifestedasbradycardia?IfbradycardiaandRSAcanbothberemovedbyseveringthevagusorbypharmacologicalblockade,aretheybothmanifestationsofvagaltone?IfbradycardiaandRSAarebothindicesofvagaltone,whydotheyresponddifferently?ThisapparentparadoxprovidesthestimulusforthefollowinginquiryandthedevelopmentoftheproposedPoly‐VagalTheorythatspeculatesthat,inmammals,therearetwoanatomicallybasedvagalresponsesystems.MammalianPoly­VagalSystemTounderstandtheproposedPoly‐VagalTheory,itisnecessarytoprovideadditionalinformationregardingtheneuroanatomyandneurophysiologyofthevagusinmammals.First,thevagusisnotonenerve,butafamilyofneuralpathwaysoriginatinginseveralareasofthebrainstem.Second,thereareseveralbranchesofthevagus.Third,thevagusisnotsolelyanefferentormotorpathway;rather,atleast80%ofthevagalfibersareafferent(Agostoni,Chinnock,DeBurghDaly,&

Murray,1957).Fourth,thevagusislateralizedwithnervetrunksoriginatingintheleftandrightsidesofthebrainstem.Fifth,thevagusisasymmetricalwiththeleftandrightsidesperformingdifferenttasks,withtherightvagusmostpotentinthechronotropicregulationoftheheart.ThesepointsaresummarizedinTable2.Table2MammalianPoly‐VagalSystem

1.Efferentfibersoriginateprimarilyintwomedullarynuclei(NA,DMNX).2.Vagalefferentfibersareclusteredintoseveralbranches.3.Approximately80%ofvagalfibersareafferent.4.Thevagusislateralized.5.Thevagusisasymmetricalwitharightbias.

Mammalsarepoly‐vagal.Thedifferentvagihavedifferentrolesintheregulationofvisceralfunctionandoriginateindifferentbrainstemnucleiwiththeirrespectiveviscerotropicorganization.Thedifferentvagimayhaveoppositionaloutputstothesametargetorgan.Forexample,itispossiblethatduringorientingthereisanincreaseinvagaloutflowfromonebranchtoproducebradycardiaandawithdrawalofvagaloutflowfromtheotherbranchtoproduceasuppressionofRSA(e.g.,RichardsandCasey,1991).Thus,theconceptofvagaltonemaynotbegeneralizedtoallvagalefferentpathwaysoreventothesametargetorgan(e.g.,heart),ashasbeenassumed(e.g.,Grossman&Kollai,1993),butmayneedtobelimitedtoaspecificbranchorsubsystemofthevagusbeingevaluated.And,theintriguingconceptofautonomicspaceproposedbyBerntson,Cacioppo,andQuigley(1991,1993)todealwithdynamicsympathetic‐parasympatheticinteractionsmayrequireanadditionaldimensiontodealwithpotentialvago‐vagalinteractions.ThePoly‐VagalTheoryproposesthatneurogenicbradycardiaandRSAaremediatedbyseparatebranchesofthevagus.Thus,thetwocommonlyused,butnotinterchangeablemeasuresofcardiacvagaltonemayrepresentdifferentdimensionsofvagaltone.Inmammals,theprimarymotorfibersofthevagusoriginatefromtwoseparateanddefinablenucleiinthemedulla:thedorsalmotornucleusofthevagus(DMNX)andthenucleusambiguus(NA).DMNXisinthedorsomedialmedulla.NAisventraltoDMNXintheventrolateralreticularformation(Warwick&Williams,1975).Thenameambiguusemphasizestheinitialdifficultiesassociatedwithdeterminingitsbordersandconnectionswithinthereticularformation(Mitchell&Warwick,1955).Athirdmedullarynucleus,locatednearDMNX,thenucleustractussolitarius(NTS),istheterminusofmanyoftheafferentpathwaystravellingthroughthevagusfromperipheralorgans.Thistrinityofneuralstructuresinthemedulla,formstheprimarycentralregulatorycomponentofthevagalsystem.TherelativelocationsofthesemedullarynucleiareillustratedinFigure1.

Figure

1 MostcellsoriginatinginDMNXprojecttosubdiaphragmaticstructures(e.g.,stomach,intestines,etc).Incontrast,onlytherostralportionofNAprovidesvagalinnervationofsubdiaphragmaticstructures(Kalia&Mesulam,1980),whilemostcellsinNAprojecttosupradiaphragmaticstructures(larynx,pharynx,softpalate,esophagus,bronchi,andheart).Neurotracingandelectrophysiologicaltechniqueswithmammalsprovideadditionalevidencethatthetwovagalnucleimayfunctionindependentlyandhavedifferentcentralconnections.Thesestudieshavedemonstratedthattherearenoapparentconnectionsbetweenthetwonuclei,althoughbothnucleihaveinputfromNTS,centralnucleusoftheamygdala,andhypothalamus,(Hopkins,1987;Leslie,Reynold,&Lawes,1992).ItiswellacceptedthatinmammalstheprimarycardioinhibitorymotoneuronsarelocatedinNA.However,motorfibersfromDMNXjointhecardiacvagus(Bennett,Ford,Kidd,&McWilliam,1984).CardioinhibitoryandbronchoconstrictorneuronslocatedinNAhavemyelinatedvagalaxonsthatconductinthefastBfiberrange(McAllen&Spyer,1976,1978).Incontrast,neuronslocatedinDMNXhaveaxonsprojectingtothecardiacvagal

branchesthatarenon‐myelinatedandconductintheslowerCfiberrange.AlthoughtherearereportsofcardioinhibitoryvagalneuronswithefferentaxonsconductingintheBfiberrangebeinglocatedinbothDMNXandNA,neuronswithaxonsconductingintheCfiberrangearerestrictedtoDMNX(Jordan,Khalid,Schneiderman&Spyer,1982).Theroleofthesenon‐myelinatedvagalfibersontheheartisnotwellunderstood.Inresearchwithcats(Ford,Bennett,Kidd,&McWilliam,1990)anddogs(Donald,Samueloff&Ferguson,1967)stimulationofthesefibersdidnotaffectheartrate.However,althoughunsubstantiatedatthistime,thefunctionofthesefibersmaybedependentupontheoutflowofthemyelinatedNAfibersandmaychangeduringconditionssuchashypoxia.Forexample,theinfluenceoftheunmyelinatedfibersontheheartmaybepotentiatedwhentheoutflowfromthemylenatedNAfibersareblocked.Incontrast,intherabbit,stimulationofthenon‐myelinatedvagalfibersresultsinheartrateslowing(Woolley,McWilliam,Ford,&Clarke,1987).ThecytoarchitectureofNAillustratesthatthedorsalportioncontainssourcenucleiforspecialvisceralefferents(i.e.,voluntarymotorfibers)andtheventralportioncontainssourcenucleiforgeneralvisceralefferents(i.e.,involuntarymotorfibers).Motorprojectionsfromthedorsalportiongototargetorgansincludingthelarynx,pharynx,softpalateandesophagus.Motorprojectionsfromtheventralportiongotoseveraltargetorgansincludingtheheart,andthebronchi.Infact,theseprojectionsaccountfortheprimarycardiacandbronchomotorpathwaysandfaroutnumberthepathwaysoriginatinginDMNX.Thereisanobviousdistinctionbetweentheviscerotropicorganizationofthetwovagalnuclei.DMNXprovidestheprimaryvagalefferentstosubdiaphragmaticorgansthatregulatedigestiveandalimentaryprocesses.Incontrast,NAprovidestheprimaryvagalefferentstothesupra‐diaphragmatictargetorgansincludingsoftpalate,pharynx,larynx,esophagus,bronchi,andheart.

ThePoly­VagalTheoryThePoly‐VagalTheoryisbasedonseveralpremises.Somearefirmlygroundedinneurophysiologicalandneuroanatomicaldataandothersaremorespeculative.ThefirstpremisearticulatestheneuralregulationofbradycardiaandRSA.Basedupontheinitialpremise,itishypothesizedthattheneurogenicbradycardiaassociatedwiththeorientingreflexaremediatedbyDMNXandthatthesuppressionofheartratevariability(i.e.,reducedamplitudeofRSA)ismediatedbyNA.Premise1:NeurogenicbradycardiaandRSAaremediatedbydifferentbranchesofthevagusandneednotrespondinconcert.PhysiologicalsupportforthehypothesisthatDMNXcancontributetoneurogenicbradycardia,independentofNA,isprovidedbylesionstudies.MachadoandBrody(1988)havereportedthatchronicbilaterallesionsofNAreducedbutdidnottotallyblockbaroreceptorreflex‐mediatedbradycardiainconsciousrats.Thus,DMNXcontainsvagalneuronscapableofproducingbradycardiawitharesponselatencyassociatedwiththebaroreceptorreflex.ThisissupportedbyJerrell,Gentile,McCabe,&Schneiderman(1986),whoarguedthatdifferentialPavlovianconditioningofbradycardiainrabbits,followingsinoaorticdenervation,wasmediatedviaDMNXpathways.Theresultsposethepossibilitythatvagalpathways,originatinginboththeDMNXandNA,havethepotentialtoinfluenceheartrate.PhylogeneticdevelopmentofthePoly‐VagalSystemInvestigationsofthephylogeneticdevelopmentofthevagusprovidesupportforthefirstpremise.Sinceourinterestsareinmammalsandspecificallyhumans,thispaperwillfocusontheevolutionofvagalregulationofcardiacfunctionfromreptilestomammals.Therearetwoquestions:1)Doreptilesproduceheartratepatternsduringorientingsimilartotheneurogenicbradycardiaobservedinmammals?2)DoreptilesproduceaphenomenonsimilartoRSA?Thephylogenyofthevagusillustratestwophenomena:one,neuroanatomical,andtheother,physiological.Onaneuroanatomicallevel,differentiationofthevisceralefferentcolumnofthevagusintoadorsalmotornucleus(i.e.,DMNX)andaventrolateralmotornucleus(i.e.,NA)isfirstseeninreptiles.Inturtles(e.g.,ChelonemydasandDomoniasubtrijuga)thereisstillaconnectionbetweenthetwonuclei,butinlizards(e.g.,Varanussalvator)andcrocodiles(e.g.,Caimancrocodilus)theseparationbetweenDMNXandNAisascompleteasitisinmammals(seeBarbas‐Henry&Lohman,1984).Behavioralorientinginreptilesischaracterizedbyafocusingofexteroceptorsandafreezingofgrossmotoractivity.Parallelingthesebehaviors,neurogenicbradycardiahavebeenobserved.Belkin(seeRegal,1978)reportedthatbradycardiaispartofafearresponseiniguanas.Additionally,McDonald(1974)reportedbrady‐cardiain

thehog‐nosedsnakeduringdeathfeigning.Mostresearchersfoundthesedataincompatiblewiththeprevalentemphasisonarousalandtheuseofheartrateasindicatorofarousal.Howcouldbradycardiareflectincreasedarousalwithinthecontextofasympatheticnervoussystemorientedarousaltheory?Incontrast,RSAhasnotbeenobservedinreptiles.Researchinvestigatingthespectralcomponentsofreptilianheartratehasfailedtoidentifyheartrateoscillationsassociatedwithventilation(GonzalezGonzalez,&deVeraPorcell,1988).Phylogeneticdevelopmentnotonlyillustrateschangesintheneuroanatomyofthevagus,butalsoparallelchangesinbehavior.Oneofthesebehavioralshiftsistheadditionofactiveorvoluntaryattentionandcomplexemotions.Inconfrontingthedefensiveworld,mammals,likereptiles,haveaninitialreflexiveresponsetonovelty,theorientingreflex.However,mammalshaveadditionalbehaviorsintheirrepertoire.Followingorindependentofreflexiveorienting,mammalsmayvoluntarilyrespondwithsustainedattentiontofosterdetailedinformationprocessing,orwithfacialexpressionsandvocalizationstofostercommunication.Thus,reptilesorient;mammalsmayfirstorientandthenelecttoattendorcommunicate.Thedifferencesbetweenthereptilianandmammaliancardiacsystemsprovidesinsightintothephylogeneticdifferencesinbehaviorssuchasreptilianorientingandmammalianattentionandemotion.Thecardiacoutputandthus,energyproductionofmammalsfarexceedsthatofreptiles.Mammalshavemetabolicdemandsfourtofivetimesthatofreptiles.ThemetaphorofamachineorvehiclehasbeenproposedbyElse&Hulbert(1981)tocomparetheefficiencyandfunctionofthemammalianandreptilianmetabolicsystems.AccordingtoElseandHulbert(1981),whenidling,theaveragemammalrequiresfourtofivetimesmorefuelthantheaverageidlingreptile,evenwhenbodyweightandambienttemperaturearecontrolled.Elaboratingonthismetaphor,reptilesrepresentvehicleswithone‐literenginesandmammalsrepresentvehicleswithfour‐orfive‐literengine.Thus,asinthestoryabouttheracebetweenthetortoiseandthehare,reptileslocomotewithareliablebutunder‐poweredengineandmammalslocomotewithasuperchargedenginethatcanfunctionforonlyshortperiodswithoutrequiringrefueling.Theenergyproductioncapacitiesofreptilesandmammalscontributetotheirrespectivelifestyles.Thereisabiasamongreptilestowardpassivefeedingstrategies.Reptilestendtobesit‐and‐waitfeeders,slowcruisers,andsluggishbrowsers.Incontrast,mammalswithfour‐chamberedhearts,canactivelyhuntandgrazeandadapttochangingenvironments(Regal,1978).Tosupporttheirbehavioralnicheandtoensuretheiradaptivesuccess,reptilesandmammalsusedifferentvagalstrategiestopromotetheirlifestyles.Beingunder‐powered,reptilesdonotmaintainavagalbrakeontheheart,whichwouldfurtherreduceenergyproductionduringunchallengedsituations.Forreptiles,duringperiodsofeitherquiescenceorapnea,usuallyassociatedwithbehavioralfreezingordiving,vagalinfluencesviaDMNXareprofoundandheartrateisevenslower.Incontrast,vagal

controloftheheartisvirtuallyremovedduringperiodsofbreathingandothermotoractivities(Belkin,1964;Jacob&McDonald,1976).Theunder‐poweredreptilesusevagalefferentsfromDMNXtothehearttodealwithspecificchallenges:toorientandfreezeinresponsetopredatororprey,andtoconserveoxygenwhilesubmergedforlengthyperiods.Incontrasttounder‐poweredreptiles,superchargedmammalsusevagalefferentsfromNAasapersistentbraketoinhibitthemetabolicpotentialofthishigh‐poweredsystem.ThehighNA‐vagaltonekeepsmammalsfrom,literally,bouncingoffwalls.Thus,incontrasttothatobservedinreptiles,inmammalsvagaltoneishighestduringunchallengedsituationssuchassleep,andvagaltoneisactivelywithdrawninresponsetoexternaldemands,includingmetabolicallydemandingstatessuchasexercise,stress,attention,andinformationprocessing.Forexample,inhumans,psychologicalstatesperceivedaslifethreatening,suchaspanicandrage,arecharacterizedbyvirtuallynoNA‐vagaltonewhenindexedwiththeamplitudeofRSA(Georgeetal.,1989).Metaphorically,andconsistentwiththemodel,antisocialandpathologicalbehavioralpatternsassociatedwithrageandhyper‐reactivitywithoutconsciousself‐regulation,havebeenlabeledreptilian.Ifterrestrialmammalsadoptedthereptilianstrategyofreflexiveincreasesinvagalactivitytoproducemassiveneurogenicbradycardia,theresultwouldbecatastrophictotheoxygen‐hungrymammaliancortexandmyocardium.Thisstrategywouldrapidlyproducecardiacischemiaandcorticalanoxia.Theresultofthissequencewouldbedeath.Althoughstilldependentonoxygen,aquaticmammalsuseadivingreflexcharacterizedbyaregulatedneurogenicbradycardiatoreducemetabolicdemands.Tosurvive,aquaticmammalshavecomplexmechanisms,notavailabletoterrestrialmammals,tomanageoxygenresourcesandshiftprioritiesforoxygenwhilesubmergedforlongperiods.Itispossiblethatformammals,duringstatesofstress,whenmetabolicdemandsaregreatandvagaltonefromNAisremoved,thatthecardiacpacemakers(S‐AandA‐V)maybepronetoneurogenicbradycardiamediatedbyDMNX.Theneurogenicbradycardiamaybemassiveandlethal.Thismaybethecaseinfetaldistress,whenbradycardiaareobservedduringhypoxicepisodes,orasafactorineithersuddeninfantdeathsyndrome(SIDS)orsuddendeathinadults.Consistentwiththismodel,ithasbeendemonstratedinthedogthatprogressiveasphyxichypoxia,notonlyelicitsincreasedcardiacvagalactivity,butthesensitivityofthesino‐atrialnodetovagalefferentinfluencesispotentiated(Potter&McCloskey,1986).Thus,duringhypoxialargebradycardiamaybemaintainedwithlimitedorreducedvagalefferentactivity.

Figure2

ThePoly‐VagalTheoryprovidesapotentialexplanationforthemassiveneurogenicbradycardiaobservedduringfetaldistressandinhighriskneonateswhohavevirtuallynoobservableRSA.Forexample,asillustratedinFigure2,whenmassivebradycardiaareobservedduringfetaldistress(a),thereisabackgroundoflowbeat‐to‐beatvariability(b).Similarly,neonateswiththelowestamplitudeRSAareatgreatestriskforapneaandbradycardia(Sostek,Glass,Molina,&Porges,1984).Thus,thediminishedvagalinfluencesfromNA,responsiblefordepressedRSA

amplitude,seemtobeassociatedwithavulnerabilitytolargeneurogenicbradycardia.PotterandMcCloskey(1986)provideanexplanationofhowdepressedCNSfunctionassociatedwithhypoxiamightresultinmassiveneurogenicbradycardia.Theyreportacomplexfeedbacksystembetweendurationofhypoxia,vagalefferentdischarge,andpotentiationofthevagaloutputontheheart.Thissystemisabletomaintainbradycardia,despitethemassivedeclineinthevagalfiringassociatedwithhypoxia,bypotentiatingtheinfluenceofthevagalfiringontheS‐Anode.Undertheseconditions,althoughthebradycardiaaremediatedthroughabranchofthevagus,themagnitudeofthebradycardiaisdeterminedbyaperipheralmechanismandnolongerreflectsacentrallymediatedvagaltone.AlthoughPotterandMcCloskeydidnotmonitorRSA,wemustassumethatRSAislowintheirpreparationbecausetheanimalswereanesthetizedpriortothesurgical,electrical,andhypoxicmanipulations,andbecausebothhypoxiaandanesthesiaareassociatedwithdepressedbeat‐to‐beatheartratevariability,includingRSA(e.g.,Donchin,etal.,1985;Nelson,1976).Additionalsupportforthisbifurcationofvagalinfluencesisdemonstratedbyelectricalstimulationofthedorsalmotornucleusintherabbit.AsillustratedinFigure3,electricalstimulationofDMNXresultsinabradycardiawithoutanincreaseinRSA.Thisisincontrasttotheeffectofstimulationoftheaorticdepressornerve,whichcom‐municateswithbothNAandDMNX.NoteinFigure4thatinasimilaranesthetizedrabbit,stimulationoftheaorticdepressornerveresultsinanincreaseinRSAandamassivebradycardia(e.g.,McCabe,Yongue,Porges,&Ackles,1984).Figure3

Figure4

ThePoly‐VagalTheoryarguesthatthevagalfibersfromtheDMNXandNAaredistinguishableinstructureandfunction.Specifically,ithasbeenarguedthatthevagalefferentfibersfromtheNAaremyelinatedandcontainarespiratoryrhythmandthevagalefferentfibersfromtheDMNXareunmyelinatedanddonotexpressarespiratoryrhythm.However,therearesomeinconsistenciesintheproposeddistinction.Forexample,ascitedabove,Jordanetal.(1982)reportedthattherearecardioinhibitoryvagalneuronsoriginatingintheDMNXwithefferentaxonsconductingintheBfiberrangeandtherefore,myelinated.Moreover,Jordanetal.reportthatthesehadarespiratoryrhythm.AlthoughtheJordanetal.findingssupporttheproposeddualsourceofvagalefferents,theirfindingsconfoundtheproposedfunctionaldistinction.ThereareseveralpotentialexplanationsfortheinconsistencyidentifiedbyJordanetal.(1982).First,maybemethod.TheJordanetal.studyusedstandardneurophysiologicalstimulationandrecordingtechniquestoidentifycellbodies.AccordingtoSchwaber(1986)manyvagalfiberspreviouslyassumedtooriginateinDMNXhavebeenidentifiedwithnewermethods,suchasretrogradelylabeledHRP,

tobelocatedinNA.Schwaber(1986)alsostatesthatsinceaxonsfromtheNApassverynearthelateralborderofDMNX,itisdifficulttostimulateorlesionDMNXwithoutNAinvolvementandconfoundingelectricalstimulationstudies.Thus,additionalresearchwithmoreaccuratelabelingtechniquesmaydemonstratethatallneuronsintheBfiberrangeoriginateinNA.OurrabbitdatareportedinFigures3and4provideadditionalsupportforthepossibilityofmislabeling.AccordingtoJordanetal.(1982)allneuronsexcitedbyaorticdepressornervestimulationproducedarespiratoryrhythmintheirongoingdischarge.Similarly,asillustratedinFigure4,stimulationoftheaorticdepressornerveresultedinbothbradycardiaandincreasedRSA.However,stimulationoftheDMNXproducedonlyanattenuatedbradycardia.ThesefindingssuggestthatvagalfibersdischargingfollowingstimulationofDMNXdidnothavearespiratoryrhythm.Moreover,thebradycardiawasimmediateandsimilarinlatencytothatobservedfollowingaorticdepressornervestimulation.However,themagnitudeofbradycardiawasabout50%ofthemagnitudeelicitedviaaorticnervestimulationthatisassumedtorecruitvagalfibersfrombothNAandDMNX.ThesefindingsaresimilartothosereportedbyMachadoandBrody(1988).AsecondpossibilityisthattherearespeciesdifferencesintheorganizationandfunctionoftheDMNX.Forexample,tofacilitatefreezingbehavior,therabbitmayhaveevolveduniquemyelinatedvagalpathwaysfromtheDMNXthatwereindependentofrespiratoryfunction.Accordingtothisexplanation,theDMNXwouldhaveBfibers,buttheywouldexpressarespiratoryrhythm.Alternatively,somemammalianspeciesmayhaveneuronsinorneartheDMNXthatarepartofacommoncardiopulmonaryoscillator(Spyer&Richter,1990).FutureresearchwilldeterminewhethertheproposedfunctionalandstructuraldistinctionsbetweenDMNXandNAefferentsarticulatedinthePoly‐VagalTheoryareaccurate.Anadditionalconcernrelatestogeneralizingacrossmammalianspecies.Mostoftheneurophysiologicalandneuroanatomicalresearchonthemammalianvagushasbeenconductedwithrat,rabbit,catanddog.Studiesinvestigatingvagalregulationwithhumanshavebeenlimitedtopharmacologicalblockadestudieswithmeasuresofperipheralphysiology.Therearefewneuroanatomicalstudiesofhumanbrainstem,however,thesestudiesareoftenconductedonpatientswhohavediedofdiseaseortrauma.Thus,onemayquestionthegeneralizabilityofapoly‐vagalmodeldevelopedfrominvestigationsofrodentbrainstemtothehuman.However,existingdataillustratesphenomenasuchasclinicalbradycardiaintheabsenceofRSAinthehumanfetus(seeFigure2),shiftsinRSAindependentofheartratechangeduringinhalantanesthesia(e.g.,Donchinetal.,1985),andshortlatencyresponsesfrombothsystems(seeFigures3and4)thatargueforapoly‐vagalsystem.VagalstrategiesinmammalsandreptilesReptilianandmammalianvagalsystemshavecontradictorystrategies.Reptilesarecharacterizedbylowambientvagaltoneandtransientincreasesinvagaltoneinresponsetoenvironmentalchallenges.Incontrast,mammalsarecharacterizedby

highambientvagaltoneandtransientdecreasesinvagaltoneinresponsetoenvironmentalchallenges.Table3VagalStrategies*AmbientStateoReptiles‐‐lowDMNXoMammals‐‐highNA/lowDMNX*ResponsetoNoveltyoReptiles‐‐increaseDMNXoMammals‐‐decreaseNA/increaseDMNXToadapttothehostileworld,thereptiles'behavioralrepertoireissurvivaldriven.Mostbehaviorsareassociatedwithforaging,stalking,andfeeding.Onlylimitedtimeandenergyarededicatedtosocialinteractionssuchasparentingandreproduction.Inthereptiles'defensiveworld,neurogenicbradycardiaareadaptiveanddonotcompromisephysiologicalstatus.Reptileshavesmallermetabolicallyactivebodyorgans,havedifferentmetabolicmechanisms,arelessoxygendependentthanmammals,andcangoforlongperiodswithoutoxygen.Incontrast,theadaptivestrategyofreptilesislethalformammals.Inthedefensiveworldofmammals,itisnecessarytoincreasemetabolicoutputtofosterfightorflightbehaviors.Therefore,reflexiveneurogenicbradycardiatonoveltyforaprolongedperiodwouldreduceoxygenresourcesandmetabolicoutputandcompromisethefightorflightpotentialofmammals.Theconsequencesofreducedoxygenresourcesalsowoulddepresscentralnervoussystemfunction,reducebehavioralcomplexityandcompetentexecutionofcomplexbehaviors,induceunconsciousness,damagevitalorgansandfinally,ifpersistent,resultindeath.Thus,thecardiaccomponentoftheorientingreflexmustbeofshortdurationandreplacedbyaphysiologicalresponsethatdoesnotcompromisetheoxygen‐needynervoussystemofmammals.ThewithdrawalofvagaltoneviaNAservesthispurpose.PhylogeneticoriginsofvagalresponsepatternsTheneurogenicbradycardiacontrolledbyDMNXandobservedinreptilesandmammalsduringorientingmayhaveevolvedfromthegustatoryresponsesystemofprimitivevertebrates.Gustationistheprimarymethodforidentifyingprey(includingotherappropriatefoodsources)andpredatorsinaquaticenvironments.Forexample,infish,anundifferentiatedvagallobecontrolsgustatory,digestive,andalimentaryprocesses(Finger&Dunwiddie,1992).Areflexiveincreaseinvagaltonewouldaffectseveralorgans:1)theheart,whereitwouldreducemetabolismandenabletheanimaltofreezemomentarily,2)theorganscontaininggustatoryreceptors,whereitwouldorienttowardsthesourceofstimulationandregulatethresholdtodetectnovelty,and3)thedigestiveandalimentarysystems,whereitwouldstimulategastricsecretionandmotility.

Withphylogeneticdevelopment,theviscerotropicorganizationofthevagalsystemhasbecomemorecomplex,andincorporatespathwaysfromothercranialnervesincludingtrigeminal,facial,accessoryandglossopharyngeal.Thus,morespecializedfunctionssuchasheadrotationtoorientsensoryreceptorstowardthesourceofstimulation,masticationtoingestfood,andsalivationtoinitiategustatoryanddigestiveprocessesareintegratedintothevagalsystem.Themotorcomponentofthevagussharesevolutionaryoriginswiththefourcranialnervesmentionedabove(trigeminal,facial,accessoryandglossopharyngeal).Thevagusnotonlyinnervatessmoothandcardiacmuscle,butsimilartotheotherfourcranialnerves,itcontainsmotorpathwaysthatinnervatesomaticmuscles.Vagalpathwaysthatinnervatesomaticmuscleoftenarenotincludedintheneurophysiologyoftheautonomicnervoussystem.Thesefibersarelabeledspecialvisceralefferentstodistinguishthemfromthemotorpathwaysinnervatingsmoothandcardiacmusclethatarelabeledgeneralvisceralefferents.Thecriticaldifferencebetweenthetwotypesofmotorpathwaysisthatsomaticmuscleregulationmaybeconsciousandvoluntary,whilesmoothmuscleregulationisreflexiveandunconscious.Sincethespecialvisceralefferentsinnervatevoluntarymuscles,usuallytheyareexcludedfromtheautonomicnervoussystem.Traditionally,onlythegeneralvisceralefferentsfrombothsympatheticandparasympatheticbranchesareusedtodefinetheautonomicnervoussystem.Thesomaticmusclesinnervatedbythefivecranialnervesarisefromthebranchialarches,embryologicallyknownastheprimitivegillarches,(Warwick&Williams,1975).Thesemusclesarecriticaltoseveralmammalianbehaviors.Forexample,thesomaticmusclesinnervatedbythetrigeminal,arisingfromthefirstbranchialarch,areinvolvedinmastication,retractionofthelowerjaw,andclosingthemouth,Thespecialvisceralefferentsfromthefacialnerve,arisingfromthesecondbranchialarch,innervatethemusclesoftheface,scalp,andnecktoenablefacialexpressions.Thefacialnervealsoinnervatesmusclesinthefloorofthemouth.Althoughthetrigeminalandfacialnervesoriginatefrombranchialarchesandhavecommunicationswiththeotherthreecranialnervesoriginatingfromthebranchialarches,thesourcenucleiofthespecialvisceralefferentsfortheglossopharyngeal,vagus,andaccessorynerveoriginateinthesamemedullarynucleus,thenucleusambiguus(NA).Thus,theefferentfiberstravelthroughthreedifferentcranialnerves,buttheyoriginateinthesamesourcenucleus.Asafunctionofphylogeneticdevelopment,thesourcenucleiforthespecialvisceralefferentpathwaysintheglossopharyngeal,vagus,andaccessorynervesmigratetoformNA.Inmammals,NAcontrolsthecomplexcoordinationofpharynx,softpalate,larynx,andesophagus.Ofspecialnotetopsychophysiologicalprocesses,thethirdgillarchalsogivesrisetothecarotidbody,containingperipheralchemosensitivereceptorssensitivetooxygenandcarbondioxidelevels,(Warwick&Williams,1975).Inaddition,theaccessorynerveprovidesfibersoriginatinginthecervicalspinalcordthatinnervatethepositioningoftheneck.Thecriticalcarotidarteries,

internaljugularveins,andvagusnervesrundeepinthesemuscles(Warwick&Williams,1975).Thus,thiscomplexalsohastheabilitytoorientvisceralreceptorsviasomaticmuscles,tocoordinatestructuresrelatedtoingestionandexpulsion,andtoregulatefacialexpressionandemotion.Thesemotornucleireceiveinputfromcortextocoordinatethesecomplexbehaviorswithcardiopulmonaryfunction.Thus,phylo‐genetically,evenwhenthegillarchesevolveintothebranchiomericmusclescommontoallmammals,oxy‐genationofbloodthroughacoordinationofbreathingandheartrateduringinteractionswiththeenvironmentremainsaprimaryfunctionalobjective.TheprocessesassociatedwithNAcontrolofsupradiaphragmaticorgansappeartobeuniquelymammalian.Forexample,thissubsystemofthevaguscoordinatesthecomplexsequenceofsucking,swallowing,andbreathingthatallowsmammalstoactivelyandvoluntarilyfeedandbreathe.Moreover,NAprovidestheprimarychronotropiccontroloftheheartandcontrolstheintonationofvocalizations.Thus,NAefferentprojectionsareinvolvedwithprocessesassociatednotonlywithfeedingandbreathing,butwithprocessesassociatedwithmovement,emotion,andcommunication.Thesebehaviorscontributetotheuniquesocialandsurvivalbehaviorsobservedinmammals.TheNA‐vagusprovidesthevagalbrakethatmammalsremoveinstantaneouslytoincreasemetabolicoutputtofosterfightorflightbehaviors.TheNA‐vagusprovidesthemotorpathwaystoshifttheintonationofvocalizations(e.g.,crypatterns)toexpressemotionandtocommunicateinternalstatesinasocialcontext.Thebehavioralderivativesofthetwobranchesofthevagus,suggestatypologyinwhichonebranchofthevagusdealswithunconsciousreflexivevegetativefunctionsandtheotherbranchofthevagusisinvolvedinmoreconscious,voluntary,flexibleandoftensocialactivities.Thereisneuroanatomicalsupportforthistypology.DMNXcontainsonlygeneralvisceralefferentsthatinnervatesmoothandcardiacmusclefibersandregulateglandularsecretion.Incontrast,NAcontainsspecialvisceralefferentsthatinnervatethesomaticmusculatureofthesoftplate,larynx,pharynx,andesophagus.SomatomotorandVisceromotor:CoupledsystemsInmammals,weobservetwoevolutionarystrategiesthatlinkautonomicfunctionwithsomaticmuscleactivity.First,thereisananatomicallinkagebetweenthesegmentationofthespinalnervesandthesympatheticchain.Thislinkageisreflectedinthemotor‐relatedincreasesinsympathetictonethathavedoggedpsychophysiologistsbyconfoundingmotorandautonomicresponses.Theevolutionofthesegmentedsympatheticnervoussystemparallelstheevolutionofvoluntarymotoractivities.Thesympatheticnervoussystemregulatesvasomotortonetodirectbloodflow,andthus,oxygen,tothespecificmusclesbeingchallenged.Additionally,therearesudomotorlinkstohydrateandprotecttheskinfromtearing.Thislinkbetweensympatheticactivityandmovementhasbeenthecornerstoneofarousaltheoryandhypotheseslinkingautonomicfunctiontotemperamentand

psychopathologies.ItwasnotmanyyearsagothatObristchallengedtheLaceynotionthatautonomicstatewasindependentofmotoractivity(i.e.,metabolicdemands).Thereisnodoubtthattheeffectsofmotoractivityareprofoundontheautonomicnervoussystem.Yet,thisprofoundeffectdoesnotmitigatetheimportanceofotherrelationshipsthatmaybesensitivetospecificpsychologicalprocesses,independentofmovement.Second,thereisananatomicallinkagebetweenthesomaticmusclesthatarisefromthecranialnucleiandparasympatheticfunction.WecanobservethisclearlyintheviscerotropicorganizationofNA.NAprovidesthesourcenucleiforsomaticmusclefibersthatinnervatelarynx,pharynx,trachea,andesophagus.Moreover,ventraltothesesourcenuclei,inanareaofthenucleusambiguusknownasNAex,aregeneralvisceralefferentsthatcontroltheresistanceofthebronchi(Haselton,Solomon,Motekaitis&Kaufman,1992)andheartrate(Bieger&Hopkins,1987).Theventralportionalsoprojectstoothervisceralorgans(e.g.,Brown,1990).Baseduponneuroanatomicalstudies,ithasbeendemonstratedthatvisceromotorfunctionsregulatedbytheventralpartofNAprovidetheparasympatheticsupportforthesomatomotorprojectionsfromNA,trigeminalandfacialnerves.Neuroanatomicalstudiessuggestthat,unlikeDMNX,whichreceivesprimarysensoryinputviaNTS,NAhasthetrigeminalnerveasanimportantsourceofsensoryinput.Moreover,therostralregionofNAcommunicateswiththefacialnucleus.ThiscouplingofNAwithfacialandtrigeminalnucleiprovidesadditionalevidenceofthecoordinationofthevisceromotorregulationviaNAwithsomatomotorfunctionssuchasswallowing(Brown,1974),sucking(Humphrey,1970),and,perhaps,facialexpressions.Thus,theorganizationofthemammalianbrainstemhasevolvedtohaveaventralvagalcomplexconsistingofNAandthenucleiofthetrigeminalandfacialnervethatco‐existswiththedorsalvagalcomplexconsistingofTheDMNXandNTSthatregulatesvegetativeprocessesandisobservedinthereptile.Tofostermotormovement,visceromotor(i.e.,autonomic)processesareassociatedwithsomatomotoractivities.Intheperipherythisisdoneprimarilybythesympatheticchainandinspecialcases,suchasthoserelatedtoreproductionandelimination,thesacralbranchoftheparasympatheticnervoussystemcontributes.However,intherostralpartofmammaliananatomy(i.e.,thehead)thesomaticmusclesthatregulatefacialexpression,mastication,vocalization,swallowing,andsuckingarematchedwithgeneralvisceralefferents,projectingfromtheventralportionofNA,thatexertpotentinfluencesontheheartandthebronchi.Thesemotorfiberseffectivelyslowheartrateandincreaserespiratoryresistancetoconserveoxygenexchange.NeuroanatomicalstudiesperformedonhumanembryosandfetusessuggestthatthesevisceromotorneuronsmayhavemigratedfromDMNX(Brown,1990).Asobservedthroughbothembryologicalresearchandphylogeneticcomparisons,inmammals,theprimitivegillarchesevolveintomusclesandnervescontrollingthe

face,bonesofthemouth,jaw,pharynx,larynx,softplate,esophagus,andtrachea.Thenervesinnervatingthesemusclesuniquelyarise,notfromtheanteriorhornsofthespinalcord,butfromthesourcenucleioffivecranialnervesreferredtoabove(trigeminal,facial,glosso‐pharyngeal,vagusandaccessory).Becauseoftheiruniqueness,thesemotorsystemsareknownasspecialvisceralefferents.And,becauseoftheirvoluntaryaspects,thesepathwayshavebeenexcludedfromtraditionalconceptsoftheautonomicnervoussystem.Facialexpressions,sucking,swallowing,andvocalizations,characteristicofmammals,reflecttheuniquemammalianadaptationofspecialvisceralefferentcontrolofthevisceralmusclesevolvingfromthebranchialarches.However,similartothesynergisticrelationshipbetweenthesympatheticnervoussystemandskeletalmusclesoftheextremities,thereisasynergisticrelationshipbetweenthetraditionalgeneralvisceralefferentsofthevagusandthesomaticmusclescontrolledbythesecranialnerves.Thus,increasedoutflowofthesesomaticmusclesproducespecificvisceralshifts.Forexample,chewingwillproducesalivationintheabsenceoffood.Additionally,headrotation,viaaccessoryspecialvisceralefferents,willimpactoncardiovascularactionviathevagus.Phylogeneticdevelopmentofthecentralnervoussystemhasprogressedinmammalstoproduceabrainwithalargeneocortex(e.g.,MacLean,1990).Theneocortexisveryvulnerabletoshiftsinoxygen.Evolutionarypressureshaveresultedinautonomicstrategiesthatoptimizetheavailabilityofoxygentothecortex.However,theseuniquelymammalianstrategiescoexistwiththeancestralreptilianstrategies.Thus,premise2isstated,consistentwithMacLean'sviewthattheadvancedmammalianbraincontainsitsphylogeneticheritage.Premise2:NeurogenicbradycardiaassociatedwithorientingareaphylogeneticvestigialrelicofthereptilianbrainandaremediatedviaDMNX.Althoughphylogeneticdevelopmenthasmodifiedseveralbrainstructures,theevolvedbrainofadvancedmammalsmaintainsseveralstructuresandsystemsthatarevirtuallyidenticaltothoseobservedinprimitivereptiles.Theseprimitivestructureshaveextensiveinterconnectionsandfunctionaldependencies,althougheachiscapableofspecificindependentfunctions.Thus,inmammals,DMNXstillmaintainsitsreptilianfunctionsoffacilitatingdigestionandslowingheartrate.Mammalsutilizeanadditionalbrainstemstructure,theNA,tosupplygeneralvisceralvagalefferentsthatprovidetheprominentcontroloftheheartandthebronchi.Thecellsoforiginofthesefibersefficientlycommunicatewithlimbic,andotherhigher,centersandallowfortheconsciousandvoluntaryselectionofnovelty.Incontrast,DMNXismoredirectlyregulatedbyhypothalamiccommunication,oftentriggeredbysurvival‐orientedstimuli(Hopkins,1987;Leslie,Reynolds,&Lawes,1992).Thus,asstatedinPremise3,theregulationofvagalefferentsbyNAmechanismscontributestothemammalianabilitytodetectnovelty,activelyengagewiththeenvironment,andsociallycommunicate.

Premise3:WithdrawalofcardiacvagaltoneviaNAmechanismsisamammalianadaptationtoselectnoveltyintheenvironment,whilecopingwiththeneedtomaintainmetabolicoutputandcontinuoussocialcommunication.Tosummarizethereptilian‐mammalianevolutionaryevidence,phylogeneticdevelopmentoftheneuralregulationoftheheartprovidesinsightsintoanapparentcontradictionorparadoxinvagalcontroloftheheart.Inmostreptilestheneuroanatomydemonstrates:1)alackofanatomicallydistinguishableboundariesbetweenDMNXandNA,and2)cardiacvagalefferentpathwaysoriginatingonlyinDMNX.Inmammalstheneuroanatomydemonstrates:1)adistinctseparationofDMNXandNA,2)cardiacvagalefferentpathwaysoriginatingprimarily(butnotexclusively)inNA,3)directneuralconnectionsbetweenthecentralnucleusoftheamygdalaandNA,and4)aclusteringofmedullaryneuronsinNAcapableofregulatingthesomaticmusclesrelatedtovocalizations,facialexpression,andtocoordinatebreathingwithsuckingandswallowing.Smartandvegetativevagi.ThePoly‐VagalTheoryproposesthattheevolutionaryshiftresultinginbothaNAthatisdistinctfromtheDMNX,andtheevolutionarydevelopmentofspecialvisceralefferentschangedtheroleofthevagus.ThegeneralvisceralefferentpathwaysfromDMNXvagusarepartofapassivereflexivemotorsystemassociatedwithvegetativefunctionandthus,avegetativevagus.ThespecialvisceralefferentpathwaysfromNAcreateanactivevoluntarymotorsystemassociatedwiththeconsciousfunctionsofattention,motion,emotion,andcommunication,andthus,asmartvagus.ThePoly‐VagalTheoryrequiresareconcep‐tualizationofthevagalsystemandtheconstructofvagaltone.TheTheoryfocusesonthecytoarchitectureofthemedullarysourcenucleiofthecranialnerves.TheTheorytakesanevolutionaryapproachandinvestigates,viaembryologyandphylogeneticcomparisons,thecommonoriginsofthespecialvisceralefferentsandfocusesonthesharedmedullarystructuresforthecellbodiesofthesefibers.TheTheoryacknowledgesthatthevagalsystemiscomplex,andshouldbeorganized,notintermsofbundlesoffibersleavingthemedulla,butratherintermsofthecommonsourcenucleiofseveralofthesepathways.Functionally,thecommonsourcenucleibothprovideacentertocoordinateandregulatethecomplexinteractionsamongvariousendorgansandarerelatedtooptimizingcardiopulmonaryfunction.Mammals,withtheiroxygen‐hungrymetabolicsystems,requireaspecialmedullarycentertocoordinatecardiopulmonaryfunctionswithbehaviorsofingestion(e.g.,mastication,salivation,sucking,swallowing),oraloresophagealexpulsion(vomiting),vocalizations(e.g.,cries,speech),emotions(e.g.,facialexpressions),andattention(e.g.,rotationofthehead).TheNAplaysthisroleandservesasthecellsoforiginofthesmartvagus.ThepotentlinkbetweenNAandcardiopulmonaryfunctionobservedinmammalsisnotobservedinreptiles.Inreptiles,whichdonot

havenervestoregulatefacialexpression,NAdoesnotplayamajorroleinviscero‐motorregulation.MedullarycontributionstoacommoncardiopulmonaryoscillatorTheNAisacontinuumofinterconnectedsub‐divisionsbeginningrostrallyatthelevelofthefacialnucleusandextendingcaudallytothespinalmedullaryjunction.AsillustratedinFigure5,theratNAhasseveralsubdivisions.Thesubdivisionsarelabeled:thecompact(NAc),semicompact(NAsc),loose(NAl)andexternal(NAex)formations(Bieger&Hopkins,1987).ThedorsaldivisionconsistsofNAc,NAsc,andNAl.Thedorsaldivisionisthesourceofspecialvisceralefferentsinnervatingthesoftpalate,pharynx,larynx,andesophagus.TheventraldivisionconsistsoftheNAexandisthesourceofgeneralvisceralefferentsinnervatingthethoracicviscera,primarilythebronchiandthesino‐atrialnode.VagalfibersoriginatinginNAexandterminatinginboththebronchi(Haseltonetal,1992)andthesino‐atrialnode(Spyer&Jordan,1987)havearespiratoryrhythm,thussuggestingthatRSAmayreflectacommonrespiratoryrhythmoriginatinginor,atleast,incorporatingNA.Figure5

Afterinvestigatingtheneuroanatomicalcentersassociatedwithlaryngeal,pulmonary,andcardiacfunction,RichterandSpyer(1990)arrivedataconvergentconclusionthatNAwasacontributortoacommonrespiratoryrhythm.Theyalsospeculatedthatmammals,withtheirgreatneedsforoxygen,haveamedullarycentertoregulatecardiopulmonaryprocesses.Theyproposedthatacommoncardiorespiratoryoscillatorevolvedtofostercoordinationamongcardiacandrespiratoryprocesses.Intheirmodeltherespiratoryrhythmisdependentonthe

interactionbetweentwogroupsofneurons,oneinNTSandtheotherinNA.Accordingly,the"common"oscillatorproducingrespiratoryfrequenciesisamanifestationofaneuralnetworkcomposedofinterneuronsbetweenareascontainingthemotoneuronsregulatingrespiratory,laryngealandcardiacfunction.NotethatthecardiorespiratoryoscillatordoesnotinvolveDMNX.Tosupporttheirhypothesestheyreportcross‐correlationalstudiesofsingleunits.Thus,NAispartofthecardiorespiratoryoscillatornetwork,andtheperiodoftheoscillationsinheartrate,(theperiodofRSA)providesavalidindexoftheoutputfrequencyofthecardiopulmonaryoscillator.Otherresearchersemphasizetheimportanceofadditionalbrainstructuresascontributorstotheregulation,ifnotthegeneration,ofacardiopulmonaryrhythm.Forexample,Harperandassociateshavedemonstratedthat"respiratoryrhythms"canbeobservedinseveralnucleiinthebrainstem,midbrainandforebrain.Harper'sgroup,employingcrosscorrelationtechniques,hasreportedunitsfiringonabreath‐by‐breathbasisinperiaqueductalgray(Ni,Zhang&Harper,1990),centralnucleusoftheamygdala(Frysinger,Zhang,&Harper,1988),hippocampus(Frysinger&Harper,1989),andtheanteriorcingulate(Frysinger&Harper,1986).Inaddition,theyhavereportedthatstimulationofamygdalacaninfluencetherespiratorycycle(Harper,Frysinger,Trelease,&Marks,1984).Thelinkbetweenbronchiandheartrateoscillations(e.g.,RSA)mediatedviaNAmayhaveafunctionalinfluenceontheoxygenationofblood.Asstatedabove,theprimaryobjectiveofthephylogeneticderivativesoftheprimitivegillarchesistomaintainoxygenation.Thus,onemightspeculatethatoscillationsinvagaltonetothebronchiandtheheartmightinfluenceoxygenation.Perhaps,coherentrhythmicshiftsbetweenbronchialtoneandheartrate,withafixedphaselag,maximizeoxygendiffusion.Toanswerthisquestion,researchwouldneedtoconfirmarelationshipbetweenoxygensaturationandRSA,independentoftheaverageheartrateandrespirationrate.Currently,onlyanecdotaldataexistthatdemonstratethatclinicalconditionsinwhichoxygensaturationislow,tendtobeconditionsinwhichRSAalsoisdepressed.Supportforthishypothesisisobtainedfromresearchdemonstratingthatvagotomydisruptstheoxygenconsumption‐oxygendeliveryrelationship(Schertel,Brourman,Klilng,Schmall,Tobias&Myerowitz,1994).MeasurementofNAstatus:QuantificationofRSAForpsychophysiologists,ourinterestisprimarilyinthebehaviorsandpsychologicalprocessesassociatedwithspecialvisceralefferents.Mostresearchhasbeendirectedtowardprocessesthatrequiretheabilitytomonitorandmediatecomplexbehaviors,suchasattention,motion,emotion,andcommunication;theseprocessesareneurophysiologicallylinkedtothespecialvisceralefferentsofNA,facial,andtrigeminalnerves.Yet,manyofusmeasureonlygeneralvisceralefferentsfromboththeparasympatheticandsympatheticbranches,althoughweareinterestedinthespecialvisceralefferentsthatregulatevocalizationsandfacialexpression.Wearenotatatotalloss,becausethereisinterneuronalcommunicationbetweenthedorsal

andventralsegmentsofNA.Thus,bythenatureoftheNAhavingthegeneralvisceralefferentsregulatingheartandbronchi,itispossibletomonitorcontinuouslythevagaloutputortonusofthesmartvagus.ThisleadsustothefourthpremiseofthePoly‐VagalTheory.Premise4:TheabilityofNAtoregulatebothspecialvisceralefferentsandgeneralvisceralefferentsmaybemonitoredbytheamplitudeofRSA.ThevagalfibersoriginatingintheNAexhaveacharacteristicrespiratoryfrequencythatreflectsawaxingandwaningofinfluence.Forexample,thevagalfibersfromNAthathaveaninhibitoryactiononthesino‐atrialnodealsowaxandwaneininhibitoryinfluenceattherespiratoryrhythmandproduceRSA.Thus,itispossibletomonitorcontinuouslythegeneralstatusofNAbyevaluatingRSA.Similarly,NAfiberstothebronchithatelevatelungresistancealsowaxandwaneintheirinhibitoryinfluence(Haseltonetal.,1992).RSAisameasureofthegeneralvisceralefferentsoftheNA,andthusisanindexofthesmartvagus.RSAisnotaglobalmeasureofvagaltoneorevenameasureof"total"vagalcontroloftheheartaspreviouslyproposed(Fouad,Tarazi,Ferrario,Fighaly,&Alicandro,1984;Katona&Jih,1975;Porges,1992).Thereareothervagalandnon‐vagalinfluencesontheheart,whichcontributetobothheartratelevelandrhythm.Forexample,thereareDMNXprojections,aswellasmonosynapticcholinergicpathwayswithintheheart,sympatheticpathways,andintrinsicfactors.However,theprimary,ifnotsole,sourceofrespiratoryrhythmsontheS‐AnodeisduetoprojectionsfromNA.ToevaluateNAregulationofthesino‐atrialnode,theparametersofRSAmustbeaccuratelyextracted.WehaveapproachedthisproblembyevaluatingtheperiodandamplitudeofRSA,independentofsloweroscillationsandtrends,viaamovingpolynomialapproach(Porges&Bohrer,1990).InourresearchwehaveobtainedcorrelationsbetweenrespirationrateandperiodofRSAapproaching1.0.ThesefindingssupportthenotionofacommoncardiorespiratoryoscillatorasdescribedbyRichterandSpyer(1990).RSA,withitsamplituderepresentingvisceromotortoneanditsperiodrepresentingthecommoncardiorespiratorydrivefrequency,isthefunctionalconsequenceoftheoutputofvagalfibersoriginatinginNAandterminatingonthesino‐atrialnode.QuantificationofRSArequiresonlyanaccuratedeterminationoftheamplitudeandperiodoftheseoscillations.Additionalexperimentalconstraintstoregulatebreathingratesmightconfoundthevisceral‐medullaryfeedbacksystemwhichdeterminescentralrespiratoryrhythms.Forexample,sincepacedbreathingrequiresanawarenessofbreathingparameters,corticalinfluencesonbrainstemstructuresmightmodulatethegainofthefeedbackandinfluencetheamplitudeofRSA.Also,pacedbreathingmayshiftrespiratoryparameters,suchasrate,amplitude,inspiration‐expirationratio,inter‐breathpause,andresistance,from

brainstemsetpoints.DatahavebeenreportedillustratingthatpacedbreathingmayinfluenceRSA(Sargunaraj,Lehrer,Carr,Hochron,&Porges,1994).Variousmanipulationsorconditionsthatdepressspecialvisceralefferents,suchasinhalantanesthesia,haveprofoundinfluencesonRSA(Donchinetal.,1985).RecoveryoffunctionofspecialvisceralefferentsisparalleledbyarecoveryofRSA.Inneurology,diagnosisisoftenbasedontheevaluationofthespecialvisceralefferents.Inourresearch,wenotedthatRSAamplitudebeforeneurosurgerywasaneffectivediagnosticofneurologicalrecoveryfollowingneurosurgery(Donchin,Constantini,Szold,Byrne,&Porges,1992).AdditionalneurologicaldatademonstrateconsistentdepressionofRSAinindividualswhoarediagnosedasbraindead(Mera,Wityk,&Porges,1995).Highriskpretermneonateshaveproblemscoordinatingbreathing,sucking,andswallowing(i.e.,processesregulatedbyNA).TheseinfantshavelowlevelsofRSA(Porges,1992).Manyoftheseinfantshaveseverebradycardia.Thebradycardiaareoftenparalleledbyapnea,andadropinavailableoxygenandmaybeassumedtoreflectneurogenicvagalregulationviaDMNX.Recall,thatthisresponse,todealwithdecreasedresources,isadaptiveforreptiles,butpotentiallylethalforthehuman.Thisalsoisobservedduringfetaldistress,whenthereisseverehypoxiaassociatedwithalossofRSAandapronouncedneurogenicbradycardia(seeabove).VagalCompetitionandAutonomicDysfunctionTheconceptofcompetitionbetweensympatheticandparasympatheticinputsiswellknown.Forexample,Levy(Vanhoutte&Levy,1979;Levy,1984)hasclearlydocumentedtheabilityofvagalefferentstoinhibitsympatheticinfluences.Similarly,Berntsonandassociateshavemodelledtheinteractionsbetweensympatheticandparasympatheticefferentstotheheart(Berntson,Cacioppo,&Quigley,1991).However,theremaybeadifferenttypeofcompetition,inwhichthetwovagalbranchesareconveyingcontradictoryinformationtothetargetorgans.Sincebothvagalpathwaysarecapableofregulatingheartrate,theremaybecompetitiononthesino‐atrialnode.Duetotherateofacetylcholinedegradationonthenodaltissue(Dexter,Levy,&Rudy,1989)thecontinuousstimulationofthesino‐atrialnodebyNApathwaysmayfunctionallyprotecttheheartfrommassiveneurogenicbradycardiamediatedbyDMNX.Thus,theobservationsofmassivepathophysiologicalbradycardiainhypoxicfetusesandneonates,whohaveverylowamplitudeRSA,mayreflectthelossofNAprotectionontheSAnode.Similarly,suddendeathfollowingexercisemightreflectasimilarprocessassociatedwiththedepressionofNAinputtofostermetabolicactivity,andasurgeofDMNXinputinresponsetodecreasedoxygenresources.Thevagalcompetitionhypothesismaybegeneralizedandtestedtoexplainotherautonomicdiseasessuchasasthma.ThevagalcompetitionhypothesisproposesthatalltargetorganswithsmoothandcardiacmusclehavedualinnervationfromboththeDMNXandNA.Currently,thishasbeendocumentedinanimalpreparationsfor

heart,lungs,esophagus,andabdominalvisceraincludingpancreas,liver,andstomach(Brown,1990).However,aswiththeheart,thetwovagalinputsmayinnervateinacontradictorymanner.JustasaDMNXsurgecoupledwithlowRSAcanresultinsuddendeath,asintheexamplesabove,bronchialasthmamaybeproducedbyasimilarmechanism.Inthecaseofasthma,NAefferentcontrolofbronchiresultsinthebronchiexhibitingarhythmicwaxingandwaningwithbreathing.ThiscontinuousstimulationofthebronchibyNApathwaysmayfunctionallyprotectthebronchifrompathophysiologicalDMNXinfluences.ItispossiblethatwithoutNAinfluences,thebronchibecomevulnerabletovagalsurgesfromDMNX.Thiswouldbeanadaptiveresponseforaprimitivebrainstemattemptingtoconserveoxygen,butitislethalfortheoxygen‐hungrymammal.Theasthmaattack,similartolethalneurogenicbradycardia,maybeaproductofaprimitivevago‐vagalreflex.Inthistypeofreflex,notonlydothemotorfibersoriginate,buttheafferentfibersterminateinDMNX.Thereisananatomicalbasisforamonosynapticvago‐vagalreflex.TherearereportsthatdendriticprocessesfromDMNXneuronsextendintotheboundariesofNTS.Thus,vagalafferentfibersmaycom‐municatedirectlywithDMNXneurons(Neuheuber&Sandoz,1986).SinceafferentsterminateinDMNX,thename"motornucleus"isnotaccurateandapreferreddesignation,"dorsalnucleusofthevagusnerve"hasbeensuggested(Nara,Goto,&Hamano,1991).Inmostvagalreflexesinvolvingthebronchi,theafferentsterminateinNTSandinfluenceNAtoprovideafailsafefeedbacksystem.BaseduponthePoly‐VagalTheory,theassumptionofvagalcompetitionpromotesthefollowingtestablehypotheses:Nucleusambiguus(Vagal)ProtectionHypothesis:VagalprojectionsoriginatinginNAandterminatinginvisceralorgansprovidetonicinfluencesthatpromotehealth,growthandrestoration.Nucleusambiguus(Vagal)Withdrawalhypothesis:RemovaloftheNA‐vagalbrakeforshortperiodsoftimepromotesmetabolicoutputtofosterlocomotion.Removaloftheseinfluencesforlongperiodsplacestheorganatrisk.EmotionThePoly‐VagalTheoryprovidesasetofpredictionsregardingtherelationbetweenautonomicresponsesandemotion.Darwincarefullydescribedfacialexpressionsastheprimarydefiningcharacteristicsofemotion.Thespecialvisceralefferents,associatedwiththefacialnerve,controlmovementsoffacialexpression.Reptilesdonothavefacialmusclesandcannotmodulatefacialexpression.ThefacialnerveinmammalsnotonlyregulatesfacialmusclesbutinteractswithNAandthevagalsystem.Thus,itislogicalthatemotionalexpression,whichrequiressomaticmusclescontrolledbyspecialvisceralefferents,islinkedtothevisceromotorregulationofcardiopulmonaryfunctionviaNAvagalefferents.Additionally,specialvisceralefferentsoriginatinginNAregulatethelarynxandcontrolintonation.Thus,thefollowingpremiseisstated.

Premise5:Emotion,definedbyshiftsintheregulationoffacialexpressionsandvocalizations,willproducechangesinRSAandbronchomotortonemediatedbyNA.Asaconstruct,emotionisheterogeneous.Therefore,correlationsbetweenspecificemotionsandphysiologicalstatesmaybeafunctionofthetypeofemotion.EvenDarwin(1872)distinguishedbetweenprimaryorneurallybasedemotionsandsocialorculturallybasedemotions.Darwin(1872)suggestedthatcertainemotionshaveastheirsubstrateaninnateneuralbasisand,becausetheseemotionsareneurallybased,theyareuniversallyexpressedandunderstoodacrosscultures.Theseprimaryemotionsincludeanger,fear,panic,sadness,surprise,interest,happiness(ecstasy),anddisgust(Ross,Homan,&Buck,1994).Sincetheprevalenthypothesessuggestastrongphysiologicalbasisforprimaryemotions,wewillfocushereonrelatingprimaryemotionstothePoly‐VagalTheory.TherearetwoimportantaspectslinkingthePoly‐VagalTheorytothestudyofemotion:first,thereisaparallelbetweencorticalasymmetryandautonomicasymmetry;second,thebranchialarcheshaveevolvedintothestructuresthatmammalsusetoexpressemotion(i.e.,facialmuscles,larynx).Theliteraturedocumentstherelationshipbetweenrightbrainfunctionandprimaryemotions(Heilman,Bowers,&Valenstein,1985).Themedullarysourcenucleiandefferentpathwaysofthevagusalsoarelateralizedwitharightbias.TherightNAviatherightcardiacvagusprovidestheprimarychronotropicoutputtotheheart.Thespecialvisceralefferents,whichprovidethebehaviorsthatareusedtodefineemotion(facialexpression,vocalization)alsohavearightbiasandarelinkedneuroanatomicallytothegeneralvisceralefferentsoriginatinginNAthatregulatethebronchiandheart;organsthatareassumedtobesensitivetoemotionandstress.Itisdifficulttopredicttheinfluenceofthisrightbiasonactualfacialexpressions.Sincethefaceiscontrolledbyuppermotorneuronsthatarecrossedandlowermotorneuronsthatareuncrossed(Rinn,1984),facialexpressionmaynotbesystematicallylateralized.Infact,researchonfacialasymmetryandemotionhasnotbeenconsistent.Therehavebeenreportsoffacialexpressionsnotbeinglateralized,beinglateralizedontheleft,andothersbeinglateralizedontheright(e.g.,Hager&Ekman,1985).Thefunctionaldominanceoftherightsideofthebraininregulatingautonomicfunctionandemotionmayhaveimplicationsforthespecializationofmotorandlanguagedominanceontheleftsideofthebrain.Therightsidedresponsibilitiesofregulatinghomeostasisandmodulatingphysiologicalstateinresponsetobothinternal(i.e.,visceral)andexternal(i.e.,environmental)feedback,maycontributetothedevelopmentofmotorandlanguagefunctionsontheleftsideofthebrain.Apartitioningofcentralcontrolofvoluntaryprocesses,independentofemotional‐homeostaticprocesseswouldenabletheindividualtoexpresscomplexvoluntarylevelsofcommunicationandmovement,viatheleftsideofthebrain,andmore

intenseemotional‐homeostaticprocesses,viatherightsideofthebrain.Iftheseprocessesarelateralized,theymighthaveadegreeofautonomousregulation.Thiswouldenablesimultaneousactivationofglobalfunctionsassociatedwithemotional‐homeostaticprocessesandlanguage‐voluntarymovementprocesses.GiventhestrongtheoreticalrelationshipsbetweenlateralizedautonomicandhemisphericfunctionandbetweentheneuronsthatcontrolRSAandtheneuronsthatcontrolfacialexpressionandvocalintonation(seeFigure5),researchshouldbedirectedatevaluatingtherelationshipbetweenRSAandtheprimaryemotions.RecallthatthesourcenucleusofthefacialnerveistheborderofNAandafferentsfromthetrigeminalnerveprovideaprimarysensoryinputtoNA.Thus,theVentralVagalComplexconsistingofNAandthenucleiofthetrigeminalandfacialnervesisclearlyrelatedtotheexpressionandexperienceofemotion.BaseduponthePoly‐VagalTheory,onewouldexpectshiftsinaffectivestatetoparallelRSA.Forexample,theelicitationofanegativeprimaryemotionwouldresultinasystematicwithdrawalofvagaltoneviaNAtopromotefightandflightlikebehaviors.Incontrast,ashifttoamorepleasantaffectivestatewouldbeassociatedwithanincreaseinRSA.AstudybyBazhenova(1995),emphasizingthedynamicsofRSAchangeduringtheshiftingaffectivestates,supportsthisspeculation.Bazhenovamanipulatedtheaffectivestateofinfantsanddemonstratedthatwhenaninfantshiftedtoamorenegativeaffectivestate,RSAdecreased.Moreover,whentheinfantshiftedtoamorepositiveaffectivestate,RSAincreasedabovetheaffectivelyneutralbaselevel.ThePoly‐VagalTheorydoesnotneglecttheimportantroleofDMNXintheemotionalexperience.Forexample,DMNXiscriticalintheregulationofdigestivepolypeptidesandgastricmotility(Uvnas‐Moberg,1989),dimensionsofphysiologicalactivitythatparallelemotiveexperiencesandstress.ConsistentwiththePoly‐VagalTheory,whichemphasizestheimportanceofNAandVVCinovertemotionalexpressivenessandregulation,theTheorywouldacknowledgetheimportanceoflessconscioussurvivalorientedprocessesthataremediatedviaDorsalVagalComplexconsistingofNTSandDMNX.AcomplementarytheoryhasbeenproposedbyUvnas‐Moberg(Uvnas‐Moberg,1987,1994).TheUvnas‐MobergtheoryemphasizestheroleofDMNXintheregulationofgastrointestinalhormonesandduringemotionalstatesincludingstress,hungerandsatiety.

SummaryandConclusionThefollowingsevenpointssummarizethePoly‐VagalTheory.1.Thevagalsystemdoesnotrepresentaunitarydimension.Thevagalsystemincludesgeneralvisceralefferentfibersregulatingsmoothandcardiacmuscle,aswellspecialvisceralefferentfibersregulatingthesomaticmusclesofthelarynx,pharynx,andesophagus.Thesesomaticmusclescontrolvocalization,suckingandswallowingandinterfacetheseprocesseswithbreathing.Thevagalsystemalsoislinkedneuroanatomicallytothesourcenucleithatcontrolfacialexpression,mastication,andheadturning.2.Therearetwovagalmotorsystems.Onevagalsystemisthevegetativevagus,whichoriginatesinthedorsalmotornucleusandisassociatedwithpassivereflexiveregulationofvisceralfunctions.Theothervagalsystemisthesmartvagus,whichoriginatesinNAandisassociatedwiththeactiveprocessesofattention,motion,emotion,andcommunication.Thetwosystemsareneuroanatomicallydistinct,havedifferentontogeneticandphylogeneticorigins,andemploydifferentadaptivestrategies.3.Inmammalstheconceptthatvagaltonerepresentsasingleorsummedsystemmayhavelimitedphysiologicalorheuristicvalue.Forexample,inmammalshightonefromthedorsalmotornucleusvagalsystemmaybelethal,while,hightonefromtheNA‐vagalsystemmaybebeneficial.BasedupontheproposedPoly‐VagalTheory,anaccuratemeasureoftheNA‐systemiscriticaltotheevaluationofpsychophysiologicalrelationships.4.ThefunctionaloutputoftheNA‐vagusontheheartmaybemonitoredviaRSA.NAispartofacommonneuronalnetworkproducingacardiorespiratoryrhythm.Thus,theoutputfromthebranchofthevagusoriginatinginNAandterminatingonthesino‐atrialnodeoftheheartconveysafrequencycommontobothrespiratoryandcardiacsystems.Incontrast,theoutputfromthedorsalmotornucleusdoesnotconveyarespiratoryrhythm.5.Themagnitudeofneurogenicbradycardiaismediatedbythedorsalmotornucleus.Rapidheartratechanges,suchasconditionedanticipatoryheartratedecelerationanddecelerationsassociatedwithorienting,areneurogenicbradycardia.Additionalneurogenicbradycardiaarereflexessuchasopto‐vagalandchemo‐vagal.IntheabsenceofNAinfluencestothesino‐atrialnode,localconditionssuchashypoxiamaygreatlypotentiatethevagaleffect.6.Thereisacommoncardiopulmonaryoscillator.ThecommonrespiratoryrhythmobservedinheartrateandbreathingisproducedbyanetworkofinterneuronslocatedinNTSandNA,whichcommunicatewiththemotorneuronsthatcontrolrespiratory,laryngeal,andcardiacfunction.

7.Primaryemotionsarerelatedtoautonomicfunction.Sincetheprimaryemotionsareoftensurvivalrelated,theymustbeintegratedintocardiopulmonaryregulation.Moreover,primaryemotionshavearighthemispherebias,ipsilateralwiththeregulatorybiasofthemedullarystructurescontrollingvisceralfunction.BaseduponthePoly‐VagalTheory,additionalhypothesesmaynowbetestedevaluatingtherelationshipbetweenRSA(themeasureofNAvagaltone)andprocessesandstatesdependentuponthecoordinationofcardiopulmonaryprocesseswiththespecialvisceralefferentsofthecranialnerves.This,ofcourse,includesallprocessesassociatedwithvocalizations,feeding,breathing,andfacialexpression.IndevelopingthePoly‐VagalTheory,themoststrikinginsightscomefromthephylogeneticapproach.NotonlydoesaphylogeneticapproachexplainthevagalparadoxintermsofthemedullarysourcenucleiofthedorsalmotornucleusandNA,butithighlightstheimportanceofoxygenneedsintheevolvingnervoussystem.Asthenervoussystemgetsmorecomplex,therearegreaterdemandsforoxygen.Oxygenneedsmayhaveprovidedamajorenvironmentalpressureleadingtotheevolutionoftheadaptiveandsophisticatedautonomicnervoussystemfoundinmammals.Thus,constructssuchasorienting,attention,emotionandstressareby‐productsoftheevolutionarypressuretooptimizeoxygenresources.

ReferencesAgostoni,E.,Chinnock,J.E.,DeBurghDaly,M.,&Murray,J.G.(1957).Functionalandhistologicalstudiesofthevagusnerveanditsbranchestotheheart,lungsandabdominalviscerainthecat.JournalofPhysiology‐London,135,182‐205.Barbas‐Henry,H.A.,&Lohman,A.H.M.(1984).ThemotornucleiandprimaryprojectionsoftheIXth,Xth,XIth,andXIIthcranialnervesinthemonitorlizard,varanusexanthematicus.TheJournalofComparativeNeurology,226,565‐579.Bazhenova,O.V.(1995).Vagaltonereactivity:Apsychophysiologicalparallelofthedynamicsofaffect.PaperpresentedattheBiennialmeetingoftheSocietyforResearchinChildDevelopment.Indianapolis,IN,March30,1995.Belkin,D.A.(1964).VariationsinheartrateduringvoluntarydivingintheturtlePseudemysconcinna.Copeia,321‐330.Bennett,J.A.,Ford,T.W.,Kidd,C.,&McWilliam,P.N.(1984).Characteristicsofcatdorsalmotorvagalmotoneuroneswithaxonsinthecardiacandpulmonarybranches.JournalofPhysiology,351,27p.Berntson,G.G.,Cacioppo,J.T.,&Quigley,K.S.(1991).Respiratorysinusarrhythmia:Autonomicorigins,physiologicalmechanisms,andpsychophysiologicalimplications.Psychophysiology,30,183‐196.Berntson,G.G.,Cacioppo,J.T.,&Quigley,K.S.(1991).Autonomicdeterminism:Themodesofautonomiccontrol,thedoctrineofautonomicspace,andthelawsofautonomicconstraint.PsychologicalReview,98,459‐487.Berntson,G.G.,Cacioppo,J.T.,&Quigley,K.S.(1993).Respiratorysinusarrhythmia:Autonomicorigins,physiologicalmechanisms,andphysiologicalimplications.Psychophysiology,30,183‐196.Berntson,G.G.,Cacioppo,J.T.,&Quigley,K.S.(1993).Cardiacpsychophysiologyandautonomicspaceinhumans:Empiricalperspectivesandconceptualimplications.PsychologicalBulletin,114,296‐322.Berntson,G.G.,Cacioppo,J.T.,&Quigley,K.S.(1994).Autonomiccardiaccontrol.I.Estimationandvalidationfrompharmacologicalblockades.Psychophysiology,31,572‐585.Bieger,D.,&Hopkins,D.A.(1987).Viscerotropicrepresentationoftheupperalimentarytractinthemedullaoblongataintherat:thenucleusambiguus.JournalofComparativeNeurology,262,546‐562.

Billman,G.E.,&DuJardin,J‐P.(1990).Dynamicchangesincardiacvagaltoneasmeasuredbytime‐seriesanalysis.AmericanJournalofPhysiology,258(HeartCirculationPhysiology27):H896‐H902.Brown,J.W.(1974).Prenataldevelopmentofthehumanchiefsensorytrigeminalnucleus.JournalofComparativeNeurology,156,307‐335.Brown,J.W.(1990).Prenataldevelopmentofthehumannucleusambiguusduringtheembryonicandearlyfetalperiods.AmericanJournalofAnatomy,189,267‐283.Byrne,E.A.,&Porges,S.W.(1993).Data‐dependentfiltercharacteristicsofpeak‐valleyrespiratorysinusarrhythmiaestimation:Acautionarynote.Psychophysiology,30,397‐404.Cacioppo,J.T.,Berntson,G.G.,Binkley,P.F.,Quigley,K.S.,Uchino,B.N.,Fieldstone,A.(1994).AutonomicCardiacControlII.Noninvasiveindicesandbasalresponseasrevealedbyautonomicblockades.Psychophysiology,31,586‐598.Cournand,A.(1979).ClaudeBernard'sContributionstoCardiacPhysiology.In:E.D.Robin(Ed),ClaudeBernardandtheInternalEnvironment.NewYork:MarcelDekker,pp.97‐121..Darrow,C.W.(1929).Differencesinthephysiologicalreactionstosensoryandideationalstimuli.PsychologicalBulletin,26,185‐201.Darrow,C.W.,Jost,H.,Solomon,A.P.,&Mergener,J.C.(1942).Autonomicindicatorsofexcitatoryandhomeostaticeffectsontheelectroencephalogram.JournalofPsychology,14,115‐130.Darwin,C.(1872).TheExpressionoftheEmotionsinManandAnimals.NewYork:D.Appleton.Dellinger,J.A.,Taylor,H.L.,&Porges,S.W.(1987).Atropinesulfateeffectsonaviatorperformanceandonrespiratory‐heartperiodinteractions.AviationSpaceEnvironmentMedicine,58,333‐338.DeMeersman,R.E.(1993).Agingasamodulatorofrespiratorysinusarrhythmia.JournalofGerontology:BiologicalSciences,48,B74‐B78.Dexter,F.,Levy,M.N.&Rudy,Y.(1989).Mathematicalmodelofthechangesinheartrateelicitedbyvagalstimulation.CirculationResearch,65,1330‐1339.Donald,D.E.,Samueloff,S.L.,&Ferguson,D.(1967).Mechanismsoftachycardiacausedbyatropineinconsciousdogs.AmericanJournalofPhysiology,212,901‐910.

Donchin,Y.,Feld,J.M.,&Porges,S.W.(1985).Respiratorysinusarrhythmiaduringrecoveryfromisoflurane‐nitrousoxideanesthesia.AnesthesiaandAnalgesia,64,811‐815.Donchin,Y.,Constantini,S.,Szold,A.,Byrne,E.A.,&Porges,S.W.(1992).Cardiacvagaltonepredictsoutcomeinneurosurgicalpatients.CriticalCareMedicine,20,941‐949.Duffy,E.(1957).Thepsychologicalsignificanceoftheconceptof"arousal"or"activation."PsychologicalReview,64,265‐275.Else,PL.&Hulbert,A.J.(1981).Comparisonofthe"mammalmachine"andthe"reptilemachine":Energyproduction.AmericanJournalofPhysiology,240,(RegulatoryIntegrativecomparativePhysiology9):R‐3‐R9.Finger,T.E.,&Dunwiddie,T.V.(1992).Evokedresponsesfromaninvitroslicepreparationofaprimarygustatorynucleus:thevagallobeofgoldfish.BrainResearch,580,27‐34.Ford,T.W.,Bennett,J.A.,Kidd,C.,&McWilliam,P.N.(1990).Neuronsinthedorsalmotorvagalnucleusofthecatwithnon‐myelinatedaxonsprojectingtotheheartandlungs.ExperimentalPhysiology.,75,459‐473.Fouad,F.M.,Tarazi,R.C.,Ferrario,C.M.,Fighaly,S.,&Alicandro,C.(1984).Assessmentofpara‐sympatheticcontrolofheartratebyanoninvasivemethod.AmericanJournalofPhysiology,246,H838‐H842.Frysinger,R.C.&Harper,R.M.(1986).Cardiacandrespiratoryrelationshipswithneuraldischargeintheanteriorcingulatecortexduringsleep‐wakingstates.ExperimentalNeurology,94,247‐263.Frysinger,R.C.&Harper,R.M.(1989).Cardiacandrespiratorycorrelationswithunitdischargeinhumanamygdalaandhippocampus.ElectroencephalographyandClinicalNeurophysiology,72,463‐470Frysinger,R.C.,Zhang,J.X.,&Harper,R,M.(1988).Cardiovascularandrespiratoryrelationshipswithneuronaldischargeinthecentralnucleusoftheamygdaladuringsleep‐wakingstates.Sleep,11,317‐332.Gellhorn,E.(1964).MotionandEmotion:Theroleofproprioceptioninthephysiologyandpathologyoftheemotions.PsychologicalReview,71,457‐472.George,D.T.,Nutt,D.J.,Walker,W.V.,Porges,S.W.,Adinoff,B.,&Linnoila,M.(1989).Lactateandhyperventilationsubstantiallyattenuatevagaltoneinnormalvolunteers:Apossiblemechanismofpanicprovocation?ArchivesofGeneralPsychiatry,46,153‐156.

Goldberger,J.J.,Ahmed,M.W.,Parker,M.A.,&Kadish,A.H.(1994).Dissociationofheartratevariabilityfromparasympathetictone.AmericanJournalofPhysiology,266(HeartCirculationPhysiology35),H2152‐H2157.GonzalezGonzalez,J.,anddeVeraPorcell,L.(1988).Spectralanalysisofheartratevariabilityoflizard,Gallotiagalloti.AmericanJournalofPhysiology,254(RegulatoryIntegrativeComparativePhysiology23)R242‐R248.Graham,F.K.,&Clifton,R.K.(1966).Heart‐ratechangeasacomponentoftheorientingresponse.PsychologicalBulletin,65,305‐320.Gribben,B.,Pickering,T.G.,Sleight,P.,&Peto,R.(1971).Effectofageandhighbloodpressureonbaroreflexsensitivityinman.CirculationResearch,29,424‐431.Grossman,P.,Karemaker,J.,&Weiling,W.Predictionoftonicparasympatheticcardiaccontrolusingrespiratorysinusarrhythmia:Theneedforrespiratorycontrol.Psychophysiology,28,201‐216.Grossman,P.,&Kollai,M.(1993).Respiratorysinusarrhythmia,cardiacvagaltone,andrespiration:Within‐andbetween‐individualrelations.Psychophysiology,30,486‐495.Hager,J.C.,&Ekman,P.(1985).Theasymmetryoffacialactionsisinconsistentwithmodelsofhemisphericspecialization.Psychophysiology,22,307‐318.Harper,R.M.,Frysinger,R.C.,Trelease,R.B.,&Marks,J.D.(1984).State‐dependentalterationofrespiratorycycletimingbystimulationofthecentralnucleusoftheamygdala.BrainResearch,306,1‐8.Haselton,J.R.,Solomon,I.C.,Motekaitis,A.M.,andKaufman,M.P.(1992).Bronchomotorvagalpreganglioniccellbodiesinthedog:Ananatomicandfunctionalstudy.JournalofAppliedPhysiology,73,1122‐1129.Heilman,K.M.,Bowers,D.,&Valenstein,E.(1985).Emotionaldisordersassociatedwithneurologicaldiseases.In:K.M.HeilmanandE.Valenstein(Eds.),Neuropsychology.NewYork:OxfordUniversityPress.Hopkins,D.A.(1987).Thedorsalmotornucleusofthevagusnerveandthenucleusambiguus:structureandconnections.InR.Hainsworth,P.N.Williams,&D.A.G.G.Many(eds.)Cardiogenicreflexes:ReportofanInternationalSymposium.Oxford:OxfordUniversityPress,pp.185‐203.Humphrey,T.(1970).Functionofthenervoussystemduringprenatallife.InU.Stave(ed.)Physiologyoftheperinatalperiod.NewYork:Appleton‐Century‐Crofts,pp.751‐796.

Jacob,J.S.,&McDonald,H.S.(1976).DivingbradycardiainfourspeciesofNorthAmericanaquaticsnakes.ComparativeBiochemistryandPhysiology.53A,69‐72.Jennings,J.R.,&McKnight,J.D.(1994).Inferringvagaltonefromheartratevariability.PsychosomaticMedicine,56,194‐194.Jerrell,T.W.,Gentile,C.G.,McCabe,P.M.,&Schneiderman,N.(1986).SinoaorticdenervationdoesnotpreventdifferentialPavlovianconditioningofbradycardiainrabbits.BrainResearch,100,3‐10.Jordan,D.,Khalid,M.E.M.,Schneiderman,N.,&Spyer,K.M.(1982).Thelocationandpropertiesofpreganglionicvagalcardiomotorneuronesintherabbit.PflugersArchiv,395,244‐250.Kaklia,M.,&Masulam,M.‐M.(1980).Brainstemprojectionsofsensoryandmotorcomponentsofthevaguscomplexinthecat.I.Laryngeal,tracheobronchial,pulmonary,cardiac,andgastrointestinalbranches.JournalofComparativeNeurology,193,467‐508.Katona,P.G.,&Jih,R.(1975).Respiratorysinusarrhythmia:Anon‐invasivemeasureofparasympatheticcardiaccontrol.JournalofAppliedPhysiology,39,801‐805.Lacey,B.C.,&Lacey,J.I.(1978).Twowaycommunicationbetweentheheartandthebrain.AmericanPsychologist,33,99‐113.Lacey,J.I.(1967).Somaticresponsepatterningandstress:Somerevisionsofactivationtheory.InM.H.Appley&R.Trumbull(Eds.),PsychologicalStress:IssuesinResearch.NewYork:Appleton‐Century‐Crofts,pp.14‐37.Leslie,R.A.,Reynolds,D.J.M.,&Lawes,I.N.C.(1992).Centralconnectionsofthenucleiofthevagusnerve.InS.Ritter,R.C.Ritter,&C.D.Barnes(Eds.).Neuroanatomyandphysiologyofabdominalvagalafferents.BocaRaton:CRCPress,pp.81‐98.Levy,M.N(1984).Cardiacsympathetic‐parasympatheticinteractions.FederationProceedings,43,2598‐2602.Lindsley,D.(1951).Emotion.InS.S.Stevens(Ed.),Handbookofexperimentalpsychology.NewYork:Wiley.Machado,B.H.,&Brody,M.J.(1988).Effectofnucleusambiguuslesiononthedevelopmentofneurogenichypertension.Hypertension,11,135‐138.MacLean,P.D.(1990).TheTriuneBraininEvolution.NewYork:PlenumPress.

Malik,M.,&Camm,J.A.(1993).Componentsofheartratevariability‐Whattheyreallymeanandwhatwereallymeasure.TheAmericanJournalofCardiology,72,821‐822.Malmo,R.B.(1959).Activation:Aneurophysiologicaldimension.PsychologicalReview,66,367‐386.McAllen,R.M.,&Spyer,K.M.(1976).Thelocationofcardiacvagalpreganglionicmotoneuronesinthemedullaofthecat.JournalofPhysiology,258,187‐204.McAllen,R.M.,&Spyer,K.M.(1978).Twotypesofvagalpreganglionicmotoneuronesprojectingtotheheartandlungs.JournalofPhysiology,282,353‐364.McCabe,P.M.,Yongue,B.G.,Porges,S.W.,&Ackles,P.K.(1984).Changesinheartperiod,heartperiodvariabilityandaspectralanalysisestimateofrespiratorysinusarrhythmiaduringaorticnervestimulationinrabbits.Psychophysiology,21,149‐158.McDonald,H.S.(1974).Bradycardiaduringdeath‐feigningofHeterodonplatyrhinosLatreille(Serpentes).JournalofHerpetolog,8,157‐164.Mera,F.,Wityk,R.,&Porges,S.W.(1995).Abnormalheartvariabilityinbrainsteminjury.PresentedattheAmericanAcademyofNeurology.Seattle,Washington,May9‐11,1995.Mitchell,G.A.G.&Warwick,R.(1955).Thedorsalvagalnucleus.ActaAnatomica,25,371‐395.Nara,T.,Goto,N.,&Hamano,S.(1991).Developmentofthehumandorsalnucleusofvagusnerve:amorphometricstudy.JournaloftheAutonomicNervousSystem,33,267‐276.Ni,H.,Zhang,J.X.,&Harper,R.M.(1990).Respiratory‐relateddischargeofperiaqueductalgrayneuronsduringsleep‐wakingstates.BrainResearch,511,319‐325.Nelson,N.M.Respirationandcirculationbeforebirth.InSmith,CA,&Nelson,NM,(eds.),Thephysiologyofthenewborninfant,4thedition.Thomas:Philadelphia;1976,15‐116.Neuheuber,W.L.,&Sandoz,P.A.(1986).Vagalprimaryafferentterminalsinthedorsalmotornucleusoftherat:Aretheymakingmonosynapticcontactsonpreganglionicefferentneurons?NeuroscienceLetters,69,126‐130.Obrist,P.A.(1976).Thecardiovascularbehavioralinteraction‐asitappearstoday.Psycho‐physiology,13,95‐107.

Obrist,P.A.(1981).CardiovascularPsychophysiology.NewYork:Plenum.Obrist,P.A.,Webb,R.A.,Sutterer,J.R.,andHoward,J.L.(1970).Thecardiac‐somaticrelationship:somereformulations.Psychophysiology6,569‐587.Porges,S.W.(1972).Heartratevariabilityanddecelerationasindexesofreactiontime.JournalofExperimentalPsychology,92,103‐110.Porges,S.W.(1986).Respiratorysinusarrhythmia:Physiologicalbasis,quantitativemethods,andclinicalimplications.InP.Grossman,K.Janssen,andD.Vaitl(eds.),CardiorespiratoryandCardiosomaticPsychophysiology.NewYork:Plenum,101‐115.Porges.S.W.(1992).VagalTone:Aphysiologicalmarkerofstressvulnerability.Pediatrics,90,498‐504.Porges,S.W.,&Bohrer,R.E.(1990).Analysesofperiodicprocessesinpsychophysiologicalresearch.InJ.T.CacioppoandL.G.Tassinary(eds.),PrinciplesofPsychophysiology:Physical,Social,andInferentialElements.NewYork:CambridgeUniversityPress,708‐753.Porges,S.W.,&Raskin,D.C.(1969).Respiratoryandheartratecomponentsofattention.JournalofExperimentalPsychology,81,497‐503.Potter,E.K.,&McCloskey,D.I.(1986).Effectsofhypoxiaoncardiacvagalefferentactivityandontheactionofthevagusnerveattheheartinthedog.JournaloftheAutonomicNervousSystem,17,325‐329.Regal,P.J.(1978)Behavioraldifferencesbetweenreptilesandmammal:Ananalysisofactivityandmentalcapabilities.InN.GreenbergandP.D.MacLean,(eds.),BehaviorandNeurologyofLizards,Rockville,MD:NationalInstituteofMentalHealth.p.183‐202.Richards,J.E.,&Casey,B.J.(1991).Heartratevariabilityduringattentionphasesinyounginfants.Psychophysiology,28,43‐53.Richter,D.W.,andSpyer,K.M.(1990).CardiorespiratoryControl.InA.D.Loewy&K.M.Spyer(eds),CentralRegulationofAutonomicFunction,.pp.189‐207.Riniolo,T.,Doussard‐Roosevelt,J.,&Porges,S.W.(1994).TherelationbetweenrespiratorysinusarrhythmiaandheartperiodduringwakingandsleepPsychophysiology,31,S81(abstract).

Rinn,W.E.(1984).Theneurophysiologyoffacialexpression:Areviewoftheneurologicalandpsychologicalmechanismsforproducingfacialexpressions.PsychologicalBulletin,95,52‐77.Ross,E.D.,Homan,R.W.&Buck,R.(1994)Differentialhemisphericlateralizationofprimaryandsocialemotions.Neuropsychiatry,neuropsychology,andbehavioralneurology,7,1‐19.Rowell,L.B.(1993).Centralcirculatoryadjustmentstodynamicexercise.InL.B.Rowell(Ed.).HumanCardiovascularControl.NewYork:OxfordPress,pp.162‐203.Sargunaraj,D.,Lehrer,P.M.,Carr,R.E.,Hochron,S.M.,&Porges,S.W.(1994).Theeffectsofpacedresistancebreathing.Psychophysiology,31,S85(abstract).Saul,J.P.,Berger,R.D.,Chen,M.H.,&Cohen,R.J.(1989).Transferfunctionanalysisofautonomicregulation.II.Respiratorysinusarrhythmia.AmericanJournalofPhysiology,256(HeartCirculationPhysiology25):H153‐H161.Schneiderman,N.(1974).Therelationshipbetweenlearnedandunlearnedcardiovascularresponses.InP.A.Obrist,A.H.Black,J.Brener,L.V.DiCara(eds.)CardiovascularPsychophysiology:Currentissuesinresponsemechanisms,biofeedback,andmethodology.Chicago:AldinePublishingCompany.pp.190‐210.Schwaber,J.S.(1986).Neuroanatomicalsubstratesofcardiovascularandemotional‐autonomicregulation.InA.Magro,W.Osswald,D.Reis&P.Vanhoutte(eds)Centralandperipheralmechanismsofcardiovascularregulation.NewYork:PlenumPress,pp.353‐384.Sokolov,E.N.(1963).PerceptionandtheConditionedReflex.Oxford:PergamonPress.Sostek,A.M.,Glass,P.,Molina,B.C.,&Porges,S.W.(1984).Neonatalvagaltoneandsubsequentsleepapneainpreterminfants.Psychophysiology,21,599.Spyer,K.M.,&Jordan,D.(1987).Electrophysiologyofthenucleusambiguus.InR.Hainsworth,P.N.Williams,&D.A.G.G.Many(eds.)Cardiogenicreflexes:ReportofanInternationalSymposium.Oxford:OxfordUniversityPress,pp.237‐249.Uvnas‐Moberg,K.(1987).Gastrointestinalhormonesandpathophysiologyoffunctionalgastrointestinaldisorders.ScandinaviaJournalofGastroenterology,22(Supplement128),138‐146.Uvnas‐Moberg,K.(1989).Gastrointestinalhormonesinmotherandinfant.ActaPediatricaScandinavia,351(Supplement),88‐93.

Uvnas‐Moberg,K.(1994).Roleofefferentandafferentvagalnerveactivityduringreproduction:Integratingfunctionofoxytocinonmetabolismandbehaviour.Psychoneuroendocrinology,19,687‐695.Vanhoutte,P.M.,&Levy,M.N.(1979)Cholinergicinhibitionofadrenergicneurotransmissioninthecardiovascularsystem.InC.McC.Brooks,K.Koizumi,&A.Sato(eds.)Integrativefunctionsoftheautonomicnervoussystem.Tokyo:UniversityofTokyoPress,159‐176.Warwick,R.&Williams,P.L.(ed).(1975)Gray'sAnatomy.Philadelphia:W.B.Saunders.Weiling,W.,vanBrederode,J.F.M.,deRijk,L.G.,Borst,C.,&Dunning,A.J.(1982).Reflexcontrolofheartrateinnormalsubjectsinrelationtoage:Adatabaseforcardiacvagalneuropathy.Diabetologia,22,163‐166.Weise,F.,&Heydenreich,F.(1991).Age‐relatedchangesofheartratepowerspectrainadiabeticmanduringorthostasis.DiabetesResearchandResearchandClinicalPractice,11,23‐32.Wolley,D.C.,McWilliam,P.N.,Ford,T.W.,&Clarke,R.W.(1987).Theeffectofselectiveelectricalstimulationonnon‐myelinatedvagalfibresonheartrateintherabbit.JournaloftheAutonomicNervousSystem,21,215‐221.Yokoyama,K,Jennings,R.,Ackles,P.,Hood,P.,&Boller,F.1987.Lackofheartratechangesduringanattention‐demandingtaskafterrighthemispherelesions.Neurology,37,624‐630.AuthorNotesThispaperisbasedonthepresidentialaddresstotheSocietyforPsychophysiologicalResearch,Atlanta,Georgia,October8,1994.Thepresidentialaddressandthepublishedmanuscriptarededicatedtothememoryofmyclosefriendandcollaborator,RobertE.Bohrer.Thetheorydescribedinthispaperevolvedfromoverthreedecadesofresearchandinteractionswithcolleaguesandstudents.Iamindebtedtofourindividualswhohaveservedasscientificguides.DavidC.Raskinintroducedmetopsychophysiology.RobertE.Bohrertutoredmeintimeseriesstatistics.AjitMaitimentoredmeintheneurophysiologyandembryologyofthebrainstem.EvgenySokolovprovidedamodelasamentorandstimulatedmetogenerateanintegrativetheory.Additionally,Ihavebeenfortunatetohaveoutstandingassociates,collaborators,andstudentsincludingOlgaBazhenova,EvanByrne,MichaelCheung,AaronChun,GeorgiaDeGangi,JanetDiPietro,YoelDonchin,JaneDoussard‐Roosevelt,NathanFox,PhilGoddard,StanleyGreenspan,SandyLarson,SusanLinnemeyer,PhilMcCabe,OxanaPlonskaia,LourdesPortales,ShawnReed,ToddRiniolo,PatSuess,andBrandonYonguewhohavecontributedtotheresearchanddevelopmentofThePoly‐Vagaltheory.An

additionalthankstoJaneDoussard‐Rooseveltwhoprovidedtheintellectualandemotionalballastinmylaboratoryduringmypresidencyandwhocontributedtothemanuscriptandtalkbyeditingearlierversionsandgeneratingthegraphics.AspecialthankstoSueCarterwhohaspatientlysupportedmyscientificcuriosityfor25yearsandwhohasprovidedseveralhelpfulcommentsintheorganizationofthemanuscript.Thepreparationofthismanuscriptwassupport,inpartbygrantHD22628fromtheNationalInstituteofChildHealthandHumanDevelopmentandbygrantMCJ240622fromMaternalandChildHealthBureau.AddressreprintrequeststoStephenW.Porges,DepartmentofHumanDevelopment,UniversityofMaryland,CollegePark,Maryland20742,oremailatporges@umdd.umd.edu.FigureCaptionsFigure1.Primarybrainstemnucleiofthevagus.Nucleiarebilateralandonlyoneofeachbilateralpairisillustrated.Figure2.(a)Bradycardiaduringfetaldistress.(b)Backgroundheartperiodvariabilityattimeofbradycardia.Figure3.BradycardiaelicitedbyelectricalstimulationoftheDMNXinananesthetizedrabbit.Figure4.Bradycardiaelicitedbyaorticdepressornervestimulationinananesthetizedrabbit.Figure5.Topographicorganizationofthenucleusambiguusintherat(Bieger&Hopkins,1987).AppendixATitleofthepaper.Thetitlewasselectedtoemphasizetheconceptthatevolutionaryprocesseshavesculptedtheneuralregulationofautonomicfunction.Notonlyhasevolutionprovidedobviousdivergencesinbehaviorandappearance,butevolutionhasimpactedontheautonomicstrategiesrelatedtothedetectionofnoveltyintheenvironment.Thefocusofthepaperwasnotdirectedatatheoryoforienting,norhasthepaperattemptedtodistinguishbetweentheautonomiccomponentsoforientingordefensivereflexes.Rather,thepaperhasfocusedontheneurogenicregulationofcardiacresponsesviatwovagalresponsessystems.Aprimitivesystemthatwehaveinheritedfromreptilesproducesarapidneurogenicbradycardiathatreducestheactivityofourcardiopulmonarysystemtoconserveoxygen.Thisisthestrategyofsitandwaitfeeders,commontoreptiles.Incontrast,theevolutionoftheenergy‐demandingmammalrequiredtwoautonomic‐behavioralshifts:1)mammalsneededtoobtaingreatamountsoffood;and2)mammalsneededtoprotecttheirnervoussystemsfromoxygenloss.Thesetwoobjectivesarelinked.Intheevolution

ofmammals,successinobtainingfoodresourceswasdependentupontheabilitytodetectthreat.Thus,mobilizationandattentionbecametwoimportantbehavioraldimensions.Unlikereptiles,whichorientinresponsetonoveltyandattackorreturntoaquiescentstateorlumberoff,mammalsorientandthenattend.Followingthisphaseofattentionamammalmayrapidlydepartorapproach(attack)withinthecontextoftheclassicfightorflightresponse.Withtheincreasingcomplexityofbehavior,thereisaparallelincreaseincomplexityintheorganizationandfunctionoftheautonomicnervoussystem.Thetitlealsointendedtoemphasizetheconceptthatevolutionhasplacedmammalsinadefensiveworld.Thesurvivalsystemsofreptilesandotherlowerphylacanbeorganizedintoorientinganddefensivedimensions.Mammals,tosurviveinthisdefensiveandreactiveworld,hadtocircumventthesepotentiallylethalreactionsofotherspecies.Theevolutionofthemammaliannervoussystemenablesmammalstorapidlyescapedangerandtouseneuralresourcesforthecomplexinformationprocessesrequiredtodetectsubtletiesintheenvironment.Moreover,evolutionpromotedadditionalmotorsystemsrelatedtocommunication.Motorsystemsdevelopedtocommunicateconditionsrelatedtosurvivalwithfacialexpressionsandvocalizationsassociatedwithprimaryemotions.Theevolutionarymodificationsnotonlyhadtocoexistwiththeoxygenhungrymetabolicsystem,butbyincreasingthecomplexityofmotorbehaviors,therewasanadditionalincreaseinoxygenneeds.Thus,thereisalinkbetweenthespecialvisceralefferentactionsregulatingthecommunicativeprocessesofemotion,andlaterlanguage,withthegeneralvisceralefferentactionsregulatingcardiopulmonaryfunction.Theabilitytodetectsubtletiesintheenvironmentcoupledwiththeabilitytocommunicatethreatorcomfortviafacialexpressionsandvocalizationscontributedtowithin‐speciessocialbehavior,parenting,andpairbonding.Thesecomplexfunctionsevolvedwhilethedemandingoxygenneedsofmammalswereprogrammedintothebackgroundofnervoussystemfunctionviatheautonomicnervoussystem.AppendixBPersonalretrospectiveIndiscussinganytheoreticalperspective,itisimportanttoplacetheideasandspeculationsinthecontextofearlierresearchconductedbytheinvestigator.Myearlyresearchfocusedontheuseofheartratemeasuresasindicatorsofattention.Whileconductingresearchformymaster'sthesis(Porges&Raskin,1969),Inotedthatattentiondemandingtasksproducedheartrateresponsepatternswithtwoprominentcharacteristics.First,heartrateexhibitedarapidtransitorydirectionalchangeinresponsetotaskonsetandstimuluschanges.Second,whensubjectsbecameinvolvedinthetaskandfocusedtheirattentiononthetaskdemands,heartratevariabilitywasreduced.Iwasintriguedwiththeseobservationsandspeculatedonthepossiblephysiologicalmechanisms.Thisevolvedintoatwo‐componenttheoryofattentioninwhichthecomponentswerelabeled"phasicororienting"and"tonicorattention"responses(Porges,1972).ThesefindingsstimulatedmetoinvestigateneuralmechanismsofheartrateregulationandtodeveloptheVagal

ToneIndex()ofRSA,whichIbelievedwouldhelpprovideinsightintothemechanismsmediatingthemoretonicsustainedattentionresponse.TheprecedingsectionsofthispaperprovidethebasisforthePoly‐VagalTheoryandenableaninterpretationofthetwoheartratecomponentsassociatedwithattention.Thefirstcomponent,associatedwithorientingandtheneurogenicbradycardia,isdeterminedreflexivelybythevegetativevagus,originatinginthedorsalmotornucleus.Thesecondcomponent,associatedwithvoluntaryengagementwiththeenvironmentanddepressionofRSA,isdeterminedbythesmartvagus,originatingintheNA.Thus,afteryearsofstudyingheartratepatterns,aspeculativetwo‐componentpsychophysiologicalmodelofattentionisevolvingintotheneuroanatomicallyandneurophysiologicallybasedPoly‐VagalTheory.