Longitudinal effects of two types of meditation training on brain responses to emotional stimuli in an ordinary, non-meditative state

Galle Desbordes1,2, Riccardo Barbieri3,4, Luca Citi3,4, Sara W. Lazar5, Lobsang Tenzin Negi6, Charles L. Raison7, Eric L. Schwartz1
1CenterforComputationalNeuroscienceandNeuralTechnology,BostonUniversity,Boston,MA;2A.A.Martinos

CenterforBiomedicalImagingandDepartmentofRadiology,MassachusettsGeneral Hospital,Boston,MA;3DepartmentofAnesthesia,CriticalCareandPainMedicine,MassachusettsGeneralHospital,Boston,MA;4DepartmentofBrainandCognitiveScience,Massachusetts 5DepartmentofPsychiatry,MassachusettsGeneralHospital,Boston,MA;6EmoryUniversity,Atlanta,GA;7UniversityofArizona,Tucson,AZ InstituteofTechnology,Cambridge,MA;

Introduction
Theamygdala hasbeenrepeatedlyimplicatedinemotional processingofbothpositiveandnegativevalencestimuli[9]. Previousstudiessuggestthatamygdala activationislowerin themeditativestate.However,thelongitudinaleffectsof meditationtrainingonamygdala responsestoemotional stimulihavenotbeenreportedwhenparticipantsareinan ordinary,nonmeditativestate.Ithasbeenproposedthat meditationtrainingmayinducelearningthatisnotstimulus ortaskspecific,butprocessspecific,andtherebymayresult inenduringchangesinmentalfunction[7,8].Inthisstudy,we investigatedhoweightweeksoftrainingineithermindful attentionmeditationorcompassionmeditationaffects amygdala responsestoemotionalstimuliandautonomic functioninginsubjectswheninanonmeditativestate.

Brain imaging assessments

Methods
fMRI experiment:Passiveviewingofemotionallyevocativestimuli Photographsofhumanbeings invarioussituations,fromthe InternationalAffectivePictureSystem(IAPS)database 3emotionalvalences:positive,negative,neutral,presentedinrandom order.Subjectsneversawthesameimagetwice Subjectsinstructions:Watchtheimagesandletyourselfreacttothem naturally. Siemens3Tscannerwith32channelheadcoil Simultaneousrecordingsofautonomicphysiologicaldata: ECG,breathingbelts,pulseoximeter,skinconductance 12subjectsineachofthe3groups(MAT,Compassion,Control) Regionofinterestanalysis Twoanatomicallydefinedregionsofinterest(ROIs),theleftandright amygdalae,wereautomaticallysegmentedfromeachsubject'shigh resolution(1x1x1mm)anatomicalscanusingtheFreeSurfer softwaresuite.

Results:TPJ
Wealsofoundthateightweeksoftraininginmeditation yieldedreduced brainactivationinthetemporoparietaljunction(TPJ)inresponseto emotionallyevocativeimagesinanordinary,nonmeditativestate:

Results:Autonomicassessments
(1)WefoundalongitudinalincreaseinHRVtotalpowerandalongitudinal decreaseinLF/HFratio(i.e.,amorepredominantvagal tone),both consistentwithimprovedautonomicfunction,inthetwomeditation groupsbutnotinthecontrolgroup,duringrest:

N =5N =3N =6

N =5N =3N =6

Longitudinalstudyofmeditation
TheCompassionAttentionLongitudinalMeditation(CALM) studyisanongoingrandomizedcontrolledtrialoftheeffects ofaneightweekmeditationtraininginterventiononhealthy adultswithoutpriormeditationexperience. 8weekintervention,2hours/week 3randomizedgroups: Compassionmeditation MindfulAttentionmeditation(a.k.a.shamatha) Activecontrol Homework:meditate2030mineveryday Nophysicalexercise(e.g.,yoga)ordietarychangeinvolved; peoplekeeptheirhabituallifestyle. Firstgroup:MindfulAttentionTraining(MAT) DesignedbyAlanWallace.Meditationpractices: Settlingthebodyandrespirationintheirnaturalstate Mindfulnessofbreathingwith relaxation stabilityofattention vividness Settlingthemindinitsnaturalstate Awarenessofawareness Secondgroup:CognitiveBasedCompassionTraining(CBCT) DesignedbyGeshe Lobsang Tenzin Negi MeditationpracticesbasedonTibetanlojong (mindtraining) techniques: Attentionandstabilityofmind,asinMAT Compassionforoneselfthroughmindfulnessofsensations, feelingsandemotions Equanimityandappreciationforothers Affectionandempathy Wishingandaspirational compassion Activecompassion Thirdgroup(controlgroup):Healthdiscussions Activecontrolintervention Alsomeetsfor2hoursaweek: Onehourtalkonahealthrelatedtopic Onehouractiveparticipationinsmallgroupdiscussions

(2)WealsofoundamarkedincreaseinRSAduringmeditationcompared torest:
RSA

Results:Amygdala
Wefoundthateightweeksoftraininginmeditation yieldedreduced brainactivationintherightamygdala inresponsetoemotionally evocativeimagesinanordinary,nonmeditativestate.Thisresultmay indicategreaterequanimityinresponsetoemotionalchallenge.In addition,inthecompassionmeditationgroup,theamygdala responseto negativevalence imagesremainedhigh(unlikeinthemindfulattention meditationgroup),perhapsindicatingthatthesubjectsexperienced increasedcompassionforhumanbeingsinsituationsofsuffering.
N =4 N =4

ThesefindingsintheTPJarecounterintuitive. TPJisinvolvedinTheoryofMind,andcognitiveperspectivetaking.Itwas aprioriexpectedthatTPJresponsetoimagesofotherpeoplewould increase(ratherthandecrease)afterCompassiontraining. Furtheranalysesofourdatawillelucidatewhathappensinotherbrain areasrelatedtoempathyandcompassion,andwhatpatternsof functionalconnectivityexistbetweenthemandTPJ.

ThesefindingssuggestthatmeasuresofRSAmightbeusefulmarkers ofthemeditativestate,andencouragefurtherinvestigationonthe efficacyofHRVmeasurestoindicateageneralimprovementof autonomichealthaftermeditationinterventions.

Conclusions
Overall,ourneuroimaging andautonomicresultssuggestthat meditationtrainingmayaffectemotionalprocessingandautonomic functionoutsideperiodsofformalmeditationpractice.Thisis consistentwiththeoverarchinghypothesisthatthecultivationof temporarymeditativestatescanresultinenduringchangesinmental andphysiologicalfunction[8].

N=12

N=12

N=12

Autonomic assessments
Measuresofheartratevariability(HRV)andrespiratorysinusarrhythmia (RSA)whicharethehealthyfluctuationsinheartratethatreflect autonomicinfluencesoncardiacactivityhavebeenproposedasindicators ofphysicalandpsychologicalhealth[1].PreviousstudiessuggestthatHRV increasesduringsomemeditativestates,butitisnotclearhowautonomic toneisaffectedeitherintheshorttermduringmeditativestates,norasa longtermresultofmeditationpractice.Herewetesttwohypotheses: (1) Eightweeksofmeditationtrainingwillimproveautonomictone,inthe formofincreasedoverallHRVanddecreasedlowfrequencyHRVto highfrequencyHRV(LF/HF)ratio;

References
[1]HeartRateVariability:StandardsofMeasurement,PhysiologicalInterpretation,andClinicalUse.Circulation 1996 Mar1;93(5):10431065. [2]Barbieri R,Matten EC,Alabi AR,BrownEN.Apointprocessmodelofhumanheartbeatintervals:newdefinitions ofheartrateandheartratevariability.AmericanJournalofPhysiologyHeartandCirculatoryPhysiology 2005;288(1):H424. [3]Barbieri R,BrownEN.Analysisofheartbeatdynamicsbypointprocessadaptivefiltering.IEEETransactionsin BiomedicalEngineering 2006;53(1). [4]ChenZ,BrownE,Barbieri R.AssessmentofAutonomicControlandRespiratorySinusArrhythmiaUsingPoint ProcessModelsofHumanHeartBeatDynamics. IEEETransactionsinBiomedicalEngineering 2009Jul;56(7):1791 802. [5]Goldin PR&GrossJJ.Effectsofmindfulnessbasedstressreduction(MBSR)onemotionregulationinsocial anxietydisorder.Emotion 2010. [6]BrefczynskiLewisJ,LutzA,SchaeferHS,LevinsonDB,andDavidsonRJ.Neuralcorrelatesofattentional expertise inlongtermmeditationpractitioners.PNAS2007. [7]LutzA,BrefczynskiLewisJ,Johnstone T,DavidsonRJ.Regulationoftheneuralcircuitryofemotionbycompassion meditation:effectsofmeditativeexpertise.PLoS One2008. [8]Slagter HA,DavidsonRJ,LutzA.Mentaltrainingasatoolintheneuroscientific studyofbrainandcognitive plasticity.FrontiersinHumanNeuroscience,5:17,2011. [9]Sergerie etal.Theroleoftheamygdala inemotionalprocessing:aquantitativemetaanalysisoffunctional neuroimaging studies.NeuroscienceandBiobehavioral Reviews2008. [10]TaylorVAetal.Impactofmindfulnessontheneuralresponsestoemotionalpicturesinexperiencedand beginnermeditators.NeuroImage 2011. [11]Weng HY&DavidsonRJ.Neuralsubstratesofcompassion.InternationalSymposiaforContemplativeStudies 2012(conferenceabstract).

Theseresultsintheamygdala areconsistentwithpreviousstudies: Beginnermeditators show lower amygdala activationinresponseto emotionalstimuliwhentheyareinameditativestateofmindful attention[5,10] Inbeginnercompassionmeditators,decreaseinamygdala is associatedwithdecreasedselfreportedarousal[11] Experiencedmeditators showlower amygdala activationinresponse toemotionalstimuliwhentheyareinameditativestateofmindful attention[6], buthigher amygdala activationwheninameditativestateofnon referential compassion[7].

(2) RSAincreasesduringthemeditationstatecomparedtorest.

Methods
Wecollectedelectrocardiogram(ECG)recordingswhilethesubjectswere lyingsupineintheMRscanner,intwodifferentconditions: atrest(forall3groups) inameditativestate(forthemindfulattentionmeditationgrouponly). WecomputedmeasuresofHRVandRSAacrossa3minuteepochusinga pointprocessmodelofheartbeatdynamics[2,3].

Supportedby:NCCAMR01AT004698andR01AT00469801A1S1,P.I.Raison;NCCAMRC1AT005728(ARRA),P.I.Schwartz;R01HL084502.ThisresearchwascarriedoutinpartattheAthinoula A.Martinos Centerfor BiomedicalImagingattheMassachusettsGeneralHospital,usingresourcesprovidedbytheCenterforFunctionalNeuroimaging Technologies,NCRRP41RR14075,S10RR021110. Contact:desbordes@gmail.com