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ContentslistsavailableatScienceDirect

Neuroscience

Letters

j ou rn a l h om epa g e :w w w . e l s e v i e r . c o m / l o c a t e / n e u l e t

Research

paper

Entrainment

of

chaotic

activities

in

brain

and

heart

during

MBSR

mindfulness

training

Junling

Gao

a,b,c

,

Jicong

Fan

a

,

Bonnie

Wai

Yan

Wu

a

,

Zhiguo

Zhang

b

,

Chunqi

Chang

d

,

Yeung-Sam

Hung

b

,

Peter

Chin

Wan

Fung

a,e

,

Hin

hung

Sik

a,∗

aCentreofBuddhistStudies,TheUniversityofHongKong,HongKong

bDepartmentofElectricalandElectronicEngineering,TheUniversityofHongKong,HongKong cAlzheimer’sDiseaseResearchNetwork,TheUniversityofHongKong,HongKong

dSchoolofBiomedicalEngineering,ShenzhenUniversity,PRChina eCentreonBehavioralHealth,TheUniversityofHongKong,HongKong

h

i

g

h

l

i

g

h

t

s

•Waveletentropyisusedtomeasurethechaoticactivities.

•Coordinationbetweenelectronicactivitiesofbrainandheart.

•MBSRmeditationcanreducethechaoticactivityofbrainwaves.

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received9August2015 Receivedinrevisedform 12November2015 Accepted4January2016 Availableonline16January2016 Keywords: MBSR EEG Waveletentropy Sourceanalysis Brain–heartcoordination

a

b

s

t

r

a

c

t

Theactivitiesofthebrainandtheheartaredynamic,chaotic,andpossiblyintrinsicallycoordinated. ThisstudyaimstoinvestigatetheeffectofMindfulness-BasedStressReduction(MBSR)programonthe chaoticityofelectronicactivitiesofthebrainandtheheart,andtoexploretheirpotentialcorrelation. Electroencephalogram(EEG)andelectrocardiogram(ECG)wererecordedatthebeginningofan8-week standardMBSRtrainingcourseandafterthecourse.EEGspectrumanalysiswascarriedout,wavelet entropies(WE)ofEEG(togetherwithreconstructedcorticalsources)andheartratewerecalculated,and theircorrelationwasinvestigated.WefoundenhancementofEEGpowerofalphaandbetawavesand loweringofdeltawavespowerduringMBSRtrainingstateascomparedtonormalrestingstate.Wavelet entropyanalysisindicatedthatMBSRmindfulnessmeditationcouldreducethechaoticactivitiesofboth EEGandheartrateasachangeofstate.However,longitudinalchangeoftraitmayneedmorelong-term training.Forthefirsttime,ourdatademonstratedthatthechaoticactivitiesofthebrainandtheheart becamemorecoordinatedduringMBSRtraining,suggestingthatmindfulnesstrainingmayincreasethe entrainmentbetweenmindandbody.The3Dbrainregionsinvolvedinthechangeinmentalstateswere identified.

©2016TheAuthors.PublishedbyElsevierIrelandLtd.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Livingorganismsarenonlinear,complexsystems,withcertain degreeofchaoticityintheirphysiologicalvariables.Forexample, theelectroencephatholography(EEG)wavesareknownfortheir dynamicactivitywithbrainnetworksoperatingbetweenorderand chaos[1].Likewise,heartratevariability(HRV)isnon-zerofora livingsubject.However,chaoticdegreemustbemaintainedata

∗ Correspondingauthor.

E-mailaddress:hinhung@hku.hk(H.h.Sik).

certainyetnotwell-knownlimitinglevel.Thelyapunovexponent (LE)ofEEGcanbeconsideredasameasureofchaoticbehavior. Previously,westrivedtoapplytheLEofEEGasaparameterto pre-dictepilepsy[2].Similarly,wealsoanalyzedthechaoticfeaturesof electrocardiogram(ECG)wavestolookforaparameter character-izingECGsignalsthatwouldlikelyleadtopre-maturedventricular contractions[3].Sincetheadventofhigh-resolutionEEGmachine (with∼100ormorechannels),anumberofmethodshavebeen developedtomeasureobjectivelythechaoticnatureofsignals.In particular,theconceptofentropyhasbeenappliedtostudythe chaoticnatureofvarioussignals.Entropydescribesthe distribu-tionprobabilityofmoleculesinafluidsysteminphysics.During

http://dx.doi.org/10.1016/j.neulet.2016.01.001

0304-3940/©2016TheAuthors.PublishedbyElsevierIrelandLtd.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense( http://creativecommons.org/licenses/by-nc-nd/4.0/).

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theevolutionofasystemofmanysignals,thedegreeof disorder-ness,whichismeasuredbyentropy,increasesingeneral[4].Since differentEEGwaveformsrepresentdifferentstatesoftheelectrical activityofthebrain,theentropyofEEGsignalssignifiesthechaotic degreeofsuchactivityasawhole,whichcannotbemeasuredbythe traditionalspectrumanalysis.Particularly,itmeasuresthechaotic leveloverdifferentscalesandhenceismoreapplicableand con-venientforanalyzingEEGdata[4].Entropymeasureshavebeen employedtostudyAD,epilepsyandanaesthesiainclinicalsettings

[5].

Neurocardiologyinmedicinesuggestsacloseinterplaybetween the heart and the brain, and cardiac afferent information can affectemotionprocessing inthebrain [6].Thereis evidenceof meditation-relatedchangeintheheartratevariability,when com-paredtopre-meditationstates[7].Anotherstudyfoundthatduring mindfulnessmeditation,thereisalsoquantitativechangeofEEG andrespirationsignals[8].However,previousstudiesmainly inves-tigatetheeffectofmeditationonthebrainortheheartseparately. Only a few studies report onbetter coordination of body and mindaftermeditationtrainingandmindfulnesspractices[9,10]. Forexample,ithasbeenshownthatintegrativebody-mind train-ing(IBMT)increasedthecorrelationbetweenfrontalmidlinetheta waveandheartratevariability(HRV),suggestingthatabetter reg-ulationofautonomicnervoussystembymidfrontalbrainregion

[10].

Themainaimsofthisinvestigationare:(i)tomeasurethepower ofthe5 standard bandsof EEGwaveforms,inorder toseethe changesbroughtbyMBSR.(ii)tomeasurethewaveletentropyof EEGbeforeandafteraneight-weekMBSRprogram,inordertofind thedifferenceinchaoticdegreeascomparedtotherest(control) state.(iii)tofindoutthe3Dsourcepositionsrelatedtotheentropy changes,basedonasourceanalysisoftheEEGactivity.(iv)to mea-surewaveletentropyoftheheartrateconcurrentlyinordertofind thechaoticchange,similarto(ii).(v)tofindifthereiscorrelation oftheentropychangesinthetwovariablesabove,inordertosee ifthereisheart–brainentrainment.

2. Materialsandmethods

2.1. Participants

Theresearchwasapproved bythelocalInstitutionalReview Board(IRB).Allparticipantsprovidedtheirwritteninformed con-sentpriortoparticipateinthisstudy.Elevenhealthyparticipants (6males, 5 females;mean age35.7year; 7 Asians and 4 Cau-casians)fromalocalMBSRcoursevoluntarilyparticipatedinthis study.Eachparticipantwaspaid200HKDfortransportationfee.All participantswereabovetheundergraduatelevel.Sixofthemhad someexperienceofmentalexercisessuchasYoga,Qigong,orother meditationmethods.Nonetheless,theyalldidnothaveexperience inMBSRandduringtheexperiment,theywererequestedtoonly practicemindfulnessbreathinglearnedfromtheMBSRcourse.The courseweretaughtfollowingthestandardMBSRprogram consist-ingofonepre-programorientationsession,eightweeklyclasses andoneall-dayclasswhentheteachergave directinstructions. Participantsalsoneededtomakestrongcommitmenttopractice 45minofMBSRtrainingeachdayashomeassignmentsfor8weeks individually,includingbodyscanningandmindfulbreathing.

Beck Depression Inventory (BDI) was used to exclude par-ticipants with depression [11]. The effectiveness of MBSR was measuredbyFiveFacetsMindfulnessQuestionnaire(FFMQ)[12]. Thesefivefacetsincludednon-judging,describing,non-reacting, actingwithawareness,andobserving.Thesub-scoresofeachfacet andatotalscorewerecalculatedforeachparticipant.TheFFMQ wasusedtomeasurethesubjectiveexperienceofmindfulness,and

inthefollowingwealsousedEEGtomeasurerelativelyobjective brainwavesassociatedwithmindfulnesspractice.

2.2. Experimentprocedure

Tenminutesofeye-closednormalrestEEGwascollectedfor eachparticipantinaquietroomandparticipantswererequested nottoruminatetoomuchorfallasleep.Theywerealsoaskedto practicemindfulbreathingfor 10min,following theteachingof theMBSRcourse.Participantswererequestednottoruminatetoo muchorfallasleep,andapost-experimentdialogshowedthatthey couldlargelyfollowtheprocedures.EEGdatawererecordedatthe beginningoftheMBSRtraining(withintwoweeks),andlessthan onemonthaftertheMBSRcourse,resultingintwodatasetsand twoconditions.Theearly-stageMBSRconditionwasnotsetbefore MBSRtrainingbutwithintwo-weekstrainingtime.Itwastoensure thatthetraineesknewtherightwaytopracticetheMBSRmindful breathingatthetimeofEEGrecording.Thesequenceof mindful-nessstateandnormalreststatewascounter-balanced,withhalf oftheparticipantsdidthemindfulnessconditionfirstandhalfdid restconditionfirst,randomly.

2.3. Dataacquisitionandanalysis

Thedatawereacquiredbya128-channelNeuroSCANsystemin aquietroom.Thesamplingratewas1000Hz.Theoriginalreference pointwasatleftmastoid,andre-referencedtobothmastoidswhen processingthedata.TheECGelectrodeswereplacedattheleftand rightinfraclavicularfossae.

ThedatawasprocessedbyEEGlab(seeSupplementarymaterials fordetails).ThespectraofEEGwerecomputedusingfastFourier transform(FFT)andthelogpowers(dB)ofdelta(1–4Hz),theta (4–8Hz),alpha(8–12Hz),beta(12–30Hz),andgamma(30–80Hz) waves were obtained. In order to evaluate thechaotic degree, waveletentropy,anentropyoftheenergiesunderdifferentscales givenbydiscretewavelettransform,oftheEEG(aswellastheir esti-matedcorticalsources)andheartratewerethencalculated(see Supplementarymaterialsfordetailsonhowtocalculatewavelet entropy). To explore the relationship between brain and heart duringtheMBSRpracticeandnormal reststates,wecalculated thelinearcorrelationcoefficient(Pearsoncoefficient)betweenthe EEG’sandtheheartrate’swaveletentropies.

3. Results

AlltheparticipantswerenotdepressedaccordingtotheirBDI scores(<13).TheFFMQdatawasshowninSupplementaryTable 1. No significant change wasfound betweenearly-stage MBSR and post-stageMBSRstages exceptforthefacetof nonreacting (p<0.05).

TherewereenhancedAlpha(8–12Hz)andBeta(12–30Hz),and reduceddeltawaves(1–4Hz)duringMBSRpracticethanduring normalrest.Theincreaseofalphawaveswasgloballysignificant, especiallyinthefrontalandoccipitallobes.Theincreaseofbeta wavewasmainlyinthefrontallobe.Decreaseddeltawavewasat central-parietalareas.However,wedidnotfindsignificantchange betweentheearly-stageandpost-stageMBSRtraining.SeeFig.1

andSupplementaryTable2.

Similartopreviousstudies[13,14],severalregionsofinterest (ROI)were selected torepresent theoccipital lobe, themiddle frontallobeandthemiddleparietallobe(seeSupplementary mate-rialforchannelsdefinedfortheseROIs).AnalysisontheseROIs showedthattheincreaseofalphawaveanddecreaseofdeltawave wereprominentallthethreeROIs,whiletheincreaseofbetawas mainlyinthefrontallobe.SeeSupplementaryTable2.

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Fig.1.Poweranalysisondifferentspectrum.Thebottomrowisthedifferencebetweenthetwostates(firstrowisNormal-Rest,secondrowisMBSRpractice)andthe correspondingT-testresults,wherethesmalldotsindicatechannelswithsignificantdifferencebetweentwostates.Thep-valueissetat<0.05,anddarkerdotimpliessmaller p-value(moresignificantdifference).

Fig.2. Thewaveletentropyanalysisintheearly-stageandpost-stageofMBSRversusnormal-restconditions.Sincetherewerenodifferencebetweentheearly-stageand post-stageMBSR,theyweremergedtogetherforcomparisoninthethirdrowforaveragemaps.Thesmalldotsindicatechannelswithsignificantdifferencebetweentwo states.Thep-valueissetat<0.05,anddarkerdotimpliessmallerp-value(moresignificantdifference).

ThewaveletentropyofEEGwasdecreasedduringMBSRpractice ascomparedtothatduringnormalrest,bothintheearly-stageand post-stageofMBSRtraining.Sincetherewasnodifferencebetween thetwostages,theyweremergedtogetherforanaveragedmapin thethirdrowinFig.2.Themainareaswithdecreasedentropywere inthefrontallobeandtheparietal-occipitallobe.

SourceanalysisontheEEGentropyimprovedthespatial resolu-tionbydeconvolvingthescalpEEGintoelectricalactivityoverthe corticalsurface[15].Itshowedthatmajorbrainregionsaffectedby MBSRmindfulnesstrainingweretheleftmiddleoccipitallobe,the

precuneus,superiortemporallobe,andtherightmiddlecingulate cortex.SeeFig.3andSupplementaryTable3.

Analysisshowednodifferenceinaverageheart ratebutthe heartrateentropywaslowerduringMBSRtraining,both atthe beginningandafterMBSRtraining,comparedwiththecontrol.See SupplementaryTable4.

Ourdatashowedthatwaveletentropyofthebrainandheart signalsweresignificantlycorrelatedduringMBSRpracticebutnot duringnormalrest.SeeFig.4.Theupperfigureshowsthe signif-icanceofentropyofEEGineachchannelandheartrateentropy.

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Fig.3.SourceanalysisonentropyshowedthatthedifferenceinEEGsourceentropy betweentwostatesofMBSRpracticeandnormalrest(p<0.001,T-test,uncorrected).

Thesignificanceofcorrelationismostprominentinthecentralpart ofthebrain.Thelowerfigureshowsthecorrelationbetweenthe averageofbrainEEGentropyofallEEGchannelsandtheheartrate entropy.

4. Discussion

Spectrumanalysisshowedthatascomparedtonormalrest,the alphawavepowerinthefrontalandoccipitallobeincreasedinboth early-stageandpoststageofMBSRtraining,whilenosignificant

dif-ferenceexistedbetweenthetwostages.Alphawavesappearwhen thebrainisfreefromsignificantsensoryinputorspecificcognitive processing,andtheyattenuatewhenthemindisengagedin men-taltasks[16].Thisresultisinlinewithamajorityofmeditation reportsofanincreasedalphawaveduringmeditation,especiallyin beginners[17].

The beta waves increased during MBSR practice, mainly in thefrontallobe. Betawavesusuallyrepresentactive concentra-tionandalertness.Theyarelinkedtowakefulnessindailymental activity,whichusuallyconsistsofongoingcognitiveand motors-ensoryactivities[18].Ontheotherhand,deltawaveswerefound todecreasemoreduringMBSRpracticethanduringnormalrest, mainlyintheoccipitalandthefrontallobe.Deltawavescommonly appearduringnon-eyemovementsleep,andmaylocallyincrease insomespecialcasessuchasbraintumor[19].Theresultsdidnot showsignificantthetaorgammawavechange.

Waveletentropy analysisonEEGshowed that duringMBSR practice,thechaoticelectronicactivitydecreasedwhencompared tothatduringthenormalreststate.Thedecreasedareascoverboth theanteriorandposteriorregionsofthebrain,andthedifference wasprominentinboththeearly-stageandpost-stageofthe train-ing.Sincenodifferenceexistedbetweenthedatafromthetwo stages,theyweremergedtogethertogetanaveragemapofMBSR stateversusthenormalreststate,resultingindecreasedentropy inmainlytheoccipitalandfrontallobes.Thetemporallobeand centralregionswerelessaffected.Giventherelativelypoorspatial resolutioninEEGmapping,weappliedsourceanalysistofurther explorethecoreregionswiththedecreasedentropy[20].Itturned outthatthemaindifferencebetweenMBSRandnormalrest condi-tionswasattheleftoccipitalandprecuneusregions.Also,theright temporalandmiddlecingulateareaswereinvolved.

Fig.4.TheentropyofwholebrainEEGiscorrelatedwiththeentropyofheartrateduringMBSRpractice(redline),whilenosuchcorrelationisobservedduringnormal-rest (blueline).ThesmalldotsindicatechannelswithsignificantcorrelationbetweenHRentropyandeachEEGchannel.(Forinterpretationofthereferencestocolorinthisfigure legend,thereaderisreferredtothewebversionofthisarticle.)

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Theoccipitallobeandparieto-occipitalareaarerelatedtothe traitofadvancedmeditators[21].Forexample,forlong-term Vipas-sanameditator,increasedgammapowerwasfoundintheoccipital lobe.Thisincreasedgammapowermaycontributetotheenhanced sensoryawarenessinthoseadvancedpractitioners[22].The occip-itallobeengagesinprocessingvisualstimuli,whiletheprecuneus areahelpsto judgethe familiarityand usefulness of perceived information.Theprecuneusalsoaidsinternallyrepresentedvisual images.Itplaysanimportantrolenotonlyinperception,memory retrieval,butalsoinworkingmemoryandattention[23].

ThegeneralguideofMBSRinstructstheparticipantstobeless reactivetoorjudgmentalofexternalorinternal stimuli,andto stabilizethehabituallywanderingmind.Wedidfindthatthe par-ticipantshadanincreasedscoreinnon-reactingfacet.Thedecrease inentropy inthesetwo areasmayindicatea detachmentfrom visualinformationpursuit,expectationandnon-judgmentduring MBSRtraining[24].

TheentropyofheartratewaslowerduringMBSRtrainingthan duringthenormalreststate.Thedifferencewassignificantbothat thebeginningofMBSRandafterMBSR.Theheartbeatisregulated bytwocompeting autonomicnervous systems,the parasympa-theticandsympatheticnervoussystem.Lessirregularityofheart rateimpliesmorerefinedbalanceofautonomicnervoussystem; i.e.,arelativelyunwaveringinteractionbetweenparasympathetic toneandsympathetictone.Theadvancedmeditatorswerefound tohavereducedECGcomplexity,asmeasuredbyShannonentropy, whilethisreductionwasnotobservedinnovicemeditators[25]. AnotherstudyonChiandKundalinimeditationfoundlesschaotic cardiacactivityduringmeditation,anditwassuggestedthat non-linearchaoticindicescanquantitativelymeasuremeditativestates

[26].

Thereductionofentropyinthebrainandtheheartactivitieswas somehowcorrelatedduringmindfulbreathing,butnotinthe nor-malreststate.Thecorrelationismostobviousinthecentralregion ofthebrainwhichconsistsofbilateralsomatosensoryregions.This findingisinlinewithapreviousreportthatmindfulnesstraining couldincreasetheactivitiesofviscerosomaticareas,includingthe somatosensoryarea,theinsulaandparietallobe[27].Ourresult suggeststhatMBSRtrainingmayinfluenceboththeautonomicand centralnervoussystems,andimprovethecoordinationofbodyand mind.Thisprocessedcouldbemediatedbythevagalnerve,which playsacentralroleinbrain–heartcoordination[28].

Astheheartratedidnotchangesignificantly,it impliesthat MBSRpracticesmaynotspecificallystrengthenthesympathetic orparasympatheticnervoussystem.Instead,MBSRtrainingmay incorporatearefinedbalanceintheregulatoryprocessesof feed-backandfeedforwardbetweentheautonomicnerves,thebrain stemandlimbicsystems,sothatheartratebecomeslesschaotic undertwocompetingsystems[29].

Thereareseverallimitationsinthisresearch.Firstthe partic-ipantnumber couldbe increased.Although theeffect of MBSR trainingonEEGissignificant,withmoreparticipants,the early-vs.post-stageseffectmightbemoresignificantinbothbehavior andEEGdata.AnotherlimitationisthatEEGsourceanalysiswas notasaccurateasotherfunctionalneuroimagingscanners.Future resting-statefunctionalmagneticresonanceimaging(fMRI)may behelpful.However,onemajordisadvantageoffMRIstudyisits noisyinterferenceonmeditation.

Conflictsofinterest

Therearenoconflictsofinterestincludinganyfinancial, per-sonal,orotherrelationshipswithpersonsororganizationsforany authorrelatedtotheworkdescribedinthisarticle.

Acknowledgements

ThisstudywassupportedbytheSPF-201209176152Fundinthe UniversityofHongKong.WethankDr.HelenMaforherteachings inthecourseandrecruitmentofMBSRparticipants.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound, intheonlineversion,athttp://dx.doi.org/10.1016/j.neulet.2016.01. 001.

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