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2013

BrainInjury,February2013; 27(2):209-222

Heartratevariability biofeedback,ex ecutivefunctioningand chronicbraininjur y

SONYAKIM

1,2 ,VANCEZEMON 1 ,MARIEM. CAVALLO 3 ,JOSEPHF. RATH 4

ROLLINMCCRATY

5 ,&FREDERICK W.FOLEY 1,2 1 FerkaufGraduateSchoolofPsycholo gy, Yeshiva University ,Bronx,NY,USA, 2

HolyNameMedical Center,

MultipleSclerosisCenter ,Teaneck, NJ,USA,

3

AHRC,TBIAdultDay Services, NewYor k,NY, USA,

4

RuskInstitute

ofRehabilitationMedicine, NewYor kUniversity Schoolof Medicine,NewYork,NY,USA,and 5

HeartMathResearch

Center,BoulderCreek,CO ,USA

(Received29March2012; accepted9September 2012)

Abstract

Primaryobjective:Todetermine ifindividualswith braininjurycan modifyheartrate variability(HRV)through biofeedback

and,ifso, enhanceitspattern toimproveemotional regulationandproblem-solving ability.

Design:A quasi-experimentaldesignwith repeatedmeasureswas employed.Thirteenindividuals aged23-63years with

severebraininjury (13-40yearspost-onset) participatingina community-basedprogrammewere enrolled.

Mainoutcomes :Response-to-treatmentwas measuredwithHRV indices,BehaviorRating Inventoryof ExecutiveFunction

(BRIEF-A-Informant)and attention/problem-solvingtests. Results:Atpost-treatment, HRVindices(Low Frequency/HighFrequency[LF/HF] andcoherenceratio) increased

significantly.IncreasedLF/HF valuesduringthe second-halfofa 10-minutesession wereassociatedwith higherattention

scores.Participantswho scoredbetter(by scoringlower)in informantratings atpre-treatmenthad highestHRVscores at

post-treatment.Accordingly, atpost-treatment,families' ratingsofparticipants' emotionalcontrolcorrelated withHRV

indices;staffs'ratings ofparticipants' workingmemorycorrelated withparticipants'HRV indices.Self-ratingsof the

BRIEF-ATaskMonitoring scaleatpost-treatment correlatedwithfamily ratingsatpre-treatment andpost-treatment.

Conclusions:Resultsdemonstrate anassociationbetween regulationofemotions/cognition andHRVtraining. Individuals

withsevere, chronicbraininjury canmodifyHRV throughbiofeedback.Future researchshouldevaluate theefficacy ofthis

approachformodifying behaviouralproblems. Keywords:Heartratevariability (HRV)biofeedback,executive functioning,braininjury

Introduction

Braininjuriesfrom manysourcescause impairments

thataffectphysical, cognitiveand psychosocial functioninginindividuals ofanyage [1-3].Also, deficitsinexecutive functioningpresent moreobsta- clestoan individual'sfullreturn tosocialfunction- ingthan physicalormedical complicationsdo[4].

Fundamentaltoexecutive functioningisself-

regulation,whichis aperson'sability toinhibit impulses,exerciserestraint, adaptas neededand turnpassiveexperience intoproductiveactivity [5-9].Asignificant deficitinself-regulation isa hallmarkofindividuals withbrain injury[10-13].

Varioustheoriesabout theunderlyingconstructs

ofexecutivefunctioning haveemergedfrom recent studiesingoal managementtraining [11,12,14], socialproblem-solvingtheory [15-18]andthe somatichypothesis[19-22]. Thecurrentstudy drawsonthe somatichypothesisand theapplication ofpsychophysiologicalmeasures inbiofeedback

Correspondence:Sonya Kim,PhD,CRC, HolyNameMedical Center,MultipleSclerosis Center,718Teaneck Road,Teaneck, NewJersey,07666, USA.

E-mail:sk519@nyu.edu

ISSN0269-9052print/ISSN 1362-301Xonline?2013InformaUK Ltd.

DOI:10.3109/02699052.2012.729292

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training,specificallyHRV, whichrefersto the variationbetweenheartbeats. Therelevantliterature showsthatheart ratevariability(HRV) isassociated withemotionsand thoughts;the literaturealso showsthatself-regulation trainingthat incorporates

HRVbiofeedbackcan improveregulation ofemo-

tionsandbehaviour and,inturn, improvecognitive functioning[23-28].

HRVtypicallyis quantifiedbymeasuring the

intervalbetweensuccessive R-wavepeaks(RR intervals)inthe electrocardiogram(ECG).Many physicalandphysiological factorsinfluencethe time betweenRRintervals. Respiratorysinusarrhythmia (RSA)refersto thecomponentof changeinRR intervalsthatis synchronizedtothe respiratorycycle [29].RSAmay beadominant componentofthe changeinthe RRintervalwhen theindividual's breathingisat anoptimalfrequency, whichis referredtoas 'resonantfrequency'[29]) - also knownas'coherence'. Thegoalof HRVbiofeedback istohelp individualsincreasethe relativeamountof

RSAinthe HRVsignal. Frombotha psychological

andphysiologicalstandpoint [27,30,31] RSAhas beenshownto bemostclosely associatedwithself- regulation.Theamplitude ofRSA tendstobe reducedin peoplewithemotional disorders;low

HRVhas beenassociatedwith panicsymptoms,

depression,poorattentional control,emotional dysregulationandinflexibility ofbehaviour[24, 32,

33].Recentfindings establishadirect connection

betweenthecentral nervoussystem(CNS) andthe autonomicnervoussystem (ANS),whichis reflected inHRV[27, 34,35];and pre-frontalactivityhas beenassociatedspecifically withvagally-mediated

HRV[36-40].

Itisimportant tonotethat thecurrentstudy relies

uponevidencethat severebrain injurycancause dysregulationof theANS[41-45]. Morespecifically, individualswithbrain injurywhosuffer fromauto- nomicdysfunctiontypically exhibitlittlemodulation ofheartrate andlowamplitude intheHRV patterns [41,46].These findingsof decreasedHRVare correlatedwith anindividual'sdeficits intasksthat involveexecutivefunction [35].Forexample,

Hansenetal. [47]foundthat individualswithgreater

HRVhadsignificantly morecorrectresponses ina

workingmemorytest andina continuousperfor- mancetest(CPT). Thegroupwith greaterHRValso demonstratedfasterreaction timethan thegroup withlow HRV.Likewise,Mezzacappa etal.'s[48] studyofchildren withemotionaland behavioural disordersfoundthat higherscoreson tasksrequiring executivecontrol - speedin responding,accuracyof responseandinhibition ofresponsein relationto changinginformation - weresignificantly associated withhigherrespiratory sinusarrhythmia(RSA).

Executivefunctioninghas beenassociatedwith

largeamplitudemodulation inHRV[31, 35,46,

49]andlarge amplitudemodulationin HRVhas

beenreferredto ascoherenceorresonance[29,50].

Maximalmodulationoccurs ataparticular 'resonant

frequency'ofthe baroreflexsystem,typically ?0.1Hertzora10second rhythm[29].As itpertainsto HRV,resonanceis thoughttoreflect abalancebetween thetwobranches (sympathetic andparasympathetic)of theautonomicnervous system(ANS).

Insum,recent evidenceindicatesthat HRVis

associatedwithcertain specificexecutivefunctions - attention,flexibilityof behaviourandcontrol of emotions[27,31, 47,48].Also, Biswasetal. [42] reportfindingsthat indicatenot onlyanassociation betweenthemagnitude ofHRVand theseverityof headinjury,but alsoanassociation betweenthe recoveryofhigher HRVlevelsand rehabilitationof theinjuredindividual. Theseassociationssuggest thatmodulationof bothefferentand afferentANS activitythroughHRV trainingcouldenhance the prefrontalcortex'srole inexecutivefunctioning and intheindividual's abilitytoself-regulate emotional responsesandbehaviour.

Withtheserecent findingsinmind, thecurrent

studyhadtwo goals:(1)to determineifindividuals withsevere,chronic braininjurycan modifyHRV throughbiofeedbacktraining; and(2)to determineif improvedHRVcoherence intheseindividuals is associatedwithimproved emotionalregulationand problem-solvingability.

Method

Participants

Participantsweredrawn fromametropolitan brain

injuryprogramme,AHRC, inNewYork City.

AHRCisa community-based,structuredday

programmethatprovides long-termrehabilitation servicesforindividuals withmoderate-to-severe braininjury.This studyincluded 13individuals withseverebrain injury(asdocumented byprior neuropsychologicalandneurological evaluations).

Thisexperimentwas astudyof the'realworld' and

thustheexclusion criteriaemployedwere minimal andflexible.Table Icontainsinformation onthe participants'injurycharacteristics (i.e.severityand cause)andwork history.Giventhe smallsamplesize ofthisstudy, mediansandinterquartile ranges( IQR) willbereported. Thegroupconsisted ofsevenmen andsixwomen (sevenwereWhite, fiveBlack and oneWhite-Hispanic)with amedianage of44years (IQR¼22).Themedian ageof onsetwas13 (IQR¼13).Medianyears sincetheparticipant's braininjurywas 23(IQR¼17.5).MedianFull Scale

IQ(FSIQ)score was62( IQR¼14.5).VerbalIQ

210S.Kimet al.

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(VIQ)medianscore was66.0( IQR¼15.75).

PerformanceIQ(PIQ) medianwas 64

(IQR¼10.5).Median yearsofeducation was12 (IQR¼2).TheirHalstead ReitanImpairmentindex medianwas1.00 (IQR¼0.10).This scoreindicates thattheparticipants asagroup werefunctioningin thesignificantlyimpaired range.As canbeseen in

TableI,for participantswitha TBIwhoserecords

wereavailablefor review,allof themrankedas severe,accordingto aconventionalclassification system[51].

Measures

Impairmentindex.Thefollowingtests wereadmin-

isteredto obtaintheImpairment Index:

FingerTappingTest, TactualPerformance Test,

SeashoreRhythm Test,SpeechSound Perception

Testandthe CategoryTest. TheImpairment

Indexiscomputed fromthe fivetestsoriginally

includedinthe Halstead-ReitanBatteryand havebeenshown tobevery sensitivetocerebral damage[52,53].

Problem-solving.HalsteadCategoryTest (HCT)

measuresan individual'sabstractionor concept- formationability, flexibilityinthe faceofcomplex andnovelproblem-solving andcapacityto learn fromexperience[53]; ithasbeen foundtohave significantassociationwith problem-solvingskills [54,55].This testiswell-established andvalidated withgoodtest-re-test reliability[56-58].A scoreof

51errorsand aboveconstitutesimpairment.

Theoriginalslide-projector versionofthe Category

Testwasused inthisexperiment.

Attention.TheIntegratedVisual andAuditory

ContinuousPerformance Test(IVAþPlusCPT)

combinesvisualand auditorystimulito examinethe levelofimpulsivity, inattentionandhyperactivity in individualsfromage 6-96;itproduces quotient scoresforimpulsivity andinattentionand hasbeen foundtodiscriminate individualswithattention disordersfromthose without.Test-re-testwith a timeintervalof 1-4weekswas foundtohave good reliability(r¼0.74,p¼0.01)[59].The primary scoreusedfor thisstudywas theFullScale

AttentionQuotient(FAQ).

Self-reportsandinfor mantreports. Awell-established instrument,theBehavior RatingInventoryof

ExecutiveFunction-AdultVersion (BRIEF-A),isa

self-reportandinformant-report measurethatcap- turesindividuals'views oftheirown executive functioningaswell astheirinformants' views(see

Rothetal. [60]forscoring informationandpsycho-

metricproperties).At Time1(pre-treatment), only theself-reportversion oftheinventory wasused.

AtTime2 (pre-treatment)andTime 3(post-

treatment),theparticipants andtheirinformants completedthisinventory.

Heartratevariability (HRV) - Electrophysiological

recordingandanalysis

Aftertheparticipants completedtheirneuropsycho-

logicaltesting,their HRVwasrecorded. Toensure thatfatiguedid notconfoundthe signalsobtained, thisrecordingusually wasmadeon adifferentday or afteralunch break.For HRVbiofeedback,

HeartMath'semWave PCwasused. HRVinthe

formofRR intervaltachogramswas measuredwith theuseof aninfraredplethysmograph sensor.The sensorwasplaced oneitherthe leftorright earlobe, whileacomputer monitordisplayed theindividual's

HRVpatternsin realtime.

TheTaskForce oftheEuropean Societyof

Cardiologyandthe NorthAmericanSociety of

PacingElectrophysiology[30] establishedstandards

forHRVrecording andmeasurement.Frequency- domainvariableswere calculatedusingnon-para- metricpowerspectral density(PSD)analysis (PSA) of5-minute-longrecordings oftheRR intervals.In thecurrentstudy, however,HRVrecordings were obtainedovera 10-minuteperiod,which was dividedinto5-minute epochs.Thislonger and dividedrecordingperiod waschosenfor several reasons.Itis importanttonote thatthisstudy was novelinat leasttwo respects:HRVbiofeedback is TableI.Injury characteristics,aetiologyand workhistory.

Variablen

Lossof consciousness

a

NotTBI-notapplicable 5

1-4weeks(severe) 2

4weeksþ(severe)4

Notavailablein medicalrecord 2

TBI MVA6 Fall1

Assault1

NotTBI

Aneurysm1

Anoxia(atbirth) 1

Ataxia,CerebralPalsy, progressivedementia 1

Braintumour2

Lawyer1

Salesman1

Collegestudent1

Noworkexperience 10

a

Loss-of-consciousnessclassification[51].

Heartratev ariabilityandexecutivefunctioning 211

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stillinthe initialstagesof beingusedin neuropsy- chologicaltestingand itsuse withapopulation like theonein thecurrentstudy isapparentlyunprece- dented.The10-minute recordingperiod offereda chanceto determinetowhat extentalonger duration ofrecordingcould affecttheperformance ofindi- vidualswithsevere braininjury.It waspossiblethat individualswithgreater cognitiveimpairments wouldneedmore timetograsp andimplement the

HRVbiofeedback strategiesthatwere beinglearned

forthefirst timeintreatment. Furthermore,dividing the10-minuteperiod intotwo5-minute epochs offeredthechance todeterminewhether individual performancechangedover time,fromthe first

5-minuteepochto thesecondone. Frequency

bandswereset accordingtothe TaskForce[30] andtheyare definedbelow.

Outliersfrom theRRintervals wereremoved

whenthey exceededthelocal medianvalueby more than200milliseconds. One-sidedpowerspectral densities(PSD)were obtainedusingthe Welch methodimplementedin MatlabR2008b(The

Mathworks,Nattick,MA). Awindowsize of64sec-

ondsanda 50%overlapwas used.Splinefitting was usedforintegration ofthe PSD.PSAprovides informationonhow thestrengthof HRVisdistrib- utedasa functionoffrequency. HRVsignalsare definedbythe followingthreefrequency bands:

Highfrequency[HF] (0.15-0.4Hz), lowfrequency

[LF](0.04-0.15Hz) andverylowfrequency[VLF] (?0.04).The totalpower(TP) includesfrequencies from0.0033-0.4Hz [30].

Arelativelysimple custom-made,in-housecode

waswrittenusing MatlabR2008b(The Mathworks,

Nattick,MA).Given therecordingperiod of5

minutes,frequencyresolution was?0.0033Hz.

Therearetwo distinctsampling rates:Oneto

sampletheraw signalforelectrocardiographic (ECG)signaland onetosample theRR-interval signal.Thesampling forthisstudy was250Hz and

1Hz,respectively.Thesesamplingrates arein

accordancewith theNyquistcriterion foreachtype ofsignal[30]. Integrationofthe powerspectrumwas smoothcurvethrough thedata.Then, followingthe recommendationssetforth bytheTask Force,power wascalculatedfor eachfrequencyband: VLF,LF,

HFandthe threepowervalues weresummedto

obtaintotalpower.

Twomeasuresof resonancewereused inthe

currentstudy:(1) ratioofthe powerofthe LFband tothepower inthe HFband(LF/HF), where higherratiosindicate greaterresonance[61]; and (2)coherenceratio definedaspeak power/total power,wherepeak powerwasdefined asthe integralofthe PSDina 0.03-widewindowcentred atthemaximal PSDvaluelocated between0.04-

0.26Hz[50].

Procedures

Allprocedureswere conductedincompliance with

theAmericanPsychological Association's(APA)

EthicalPrinciples intheConductofResearchwith

HumanPar ticipants[62].TheAlbert Einstein

CollegeofMedicine ofYeshiva University's

InstitutionalReview Boardandthe AHRC

InstitutionalReview Boardbothapproved the

study.Aninformed consentform wasreadand signedbyall potentialparticipants.Where applica- ble,asigned AuthorizationtoUse orDisclose

ProtectedHeathInformation foraResearch Study

formwasobtained fromtheparticipants' 'advocate'.

Thisstudyfeatured asingle-treatment,non-

randomized,unblinded quasi-experimentaldesign withmeasuresrepeated atthree timepoints:Pre- treatmenttest(Time 1),pre-treatmenttest (Time2) andapost-treatment test(Time3). Inthisdesign, thetwopre-treatment timesservedas baselines againstwhichthe post-treatmentscores werecom- paredandserved tocontrolfor theeffectsof time andpractice.Testing ateachtime pointincluded

5-6hoursof neuropsychologicaltestingand com-

pletionofself-reports. Informantscompletedreports andquestionnaireson theparticipantsat Times2 and3.Recording oftheparticipants' HRVforTimes

1,2and 3wasdone duringseparatesessions, within

2daysof neuropsychologicaltesting. Times1and 2

wereseparatedby a10-weekwaiting period.

Followingbaselinetesting, theparticipantsreceived

thespeciallytailored HRVbiofeedbacksessions. The participantswerepaid $10forparticipating ineach

5-6hourtesting session,$5for completingaddi-

tionalquestionnairesafter treatmentendedand $5 foreachindividual session.Theyalso received$5 extraforattaining biofeedback'rewardcycles' usingquotesdbs_dbs44.pdfusesText_44

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