MBSR vs. AE in Social Anxiety 1 MBSR vs. Aerobic Exercise in Social Anxiety

35 Pages·2012·0.3 MB·English

doi:10.1093/scan/nss054 SCAN(2013)8,65^72
MBSR vs aerobic exercise in social anxiety:
fMRI of emotion regulation of negative self-beliefs
Philippe Goldin, Michal Ziv, Hooria Jazaieri, Kevin Hahn, and James J. Gross
Department of Psychology, StanfordUniversity, Stanford, CA,94305, USA
Mindfulness-basedstressreduction(MBSR)isthoughttoreduceemotionalreactivityandenhanceemotionregulationinpatientswithsocialanxiety
disorder(SAD).Thegoalofthisstudywastoexaminetheneuralcorrelatesofdeployingattentiontoregulateresponsestonegativeself-beliefsusing
functional magnetic resonance imaging. Participants were 56 patients with generalized SAD in a randomized controlled trial who were assigned to
MBSRoracomparisonaerobicexercise(AE)stressreductionprogram.ComparedtoAE,MBSRyieldedgreater(i)reductionsinnegativeemotionwhen
implementingregulationand(ii)increasesinattention-relatedparietalcorticalregions.Meditationpracticewasassociatedwithdecreasesinnegative D
o
emotion and social anxiety symptom severity, and increases in attention-related parietal cortex neural responses when implementing attention w
n
regulationofnegativeself-beliefs.ChangesinattentionregulationduringMBSRmaybeanimportantpsychologicalfactorthathelpstoexplainhow lo
a
mindfulnessmeditationtrainingbenefitspatientswithanxietydisorders. d
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Keywords: social anxiety; emotionregulation; mindfulness; fMRI;attention m
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INTRODUCTION There are a variety of emotion regulation strategies (Gross, 2007) ://ac
a
Mindfulness meditation is a form of mental training that has existed with distinct neural circuitry and temporal features (Goldin et al., de
m
for more than two and a half millennia in the East and has recently 2008).However,littleisknownabouthowMBSRinfluencesemotion ic
become integrated into Western health care approaches (Chiesa and regulationabilities(Chambersetal.,2009).Preliminaryevidencesug- .ou
Serretti, 2011). Mindfulness-Based Stress Reduction (MBSR; gests that MBSR may influence the ability to exert cognitive control p.c
Kabat-Zinn, 1990), the format of mindfulness training that has overnegativerumination(Rameletal.,2004),self-referentialprocesses om
received the most empirical investigation, has been shown to reduce (Goldinetal.,2009c)andattentionallocationandregulation(Slagter /sc
sMvyamBriSeptRtyomhoafsspobsfyeceshntroelasopsg,picldiaeeldp[reea.ssgs.iaoannnxaalinteetdrynaaanntixdvieedtycelpi(nrHeicsosafilmonianntdenirsvoeertndateilro.s,n2(A0fo1lrl0e)na. tedhtiseaerlne.,bgya2g0er0e8ad)tut.ecInimntigpoonermftraoonmttiloyan,vaMelrBsrieSvaRectemimviaotyytiboaennadrlesleatnitmehdaunltico(inLgguretazthteeetraaalbb.,iil2liit0tyy08tt)oo; an/article
implement emotion regulation strategies. -a
et al., 2006; Carmody, 2009; Chiesa and Serretti, 2009)] and chronic b
s
medical problems (Merkes, 2010). tra
Recently, researchers have begun to examine the mechanisms of MBSR and SAD ct/8
actionunderlyingMBSR.Onecandidatemechanismisemotionregu- One clinical context for examining the effects of MBSR on emotion /1
/6
lation, a key feature of mood and anxiety disorders and a popular regulationisSAD.SADisacommon,chronicandinsidiouspsychiatric 5
/1
target of many psychosocial clinical interventions (Campbell-Sills conditioncharacterizedbyintensefearofevaluationandavoidanceof 6
9
andBarlow,2007).Recentstudieshavefoundthatemotionregulation socialorperformancesituations(SteinandStein,2008).SADinvolves 47
8
may(i)berelatedtodispositionalmindfulness(Modinosetal.,2010) a distorted attentional focus on internal cues (e.g. negative thoughts 4
b
and(ii)enhancedwithMBSR(GoldinandGross,2010).Inthepresent and self-imagery) and external cues (e.g. other’s facial expressions) y
g
study, we used functional magnetic resonance imaging (fMRI) to in- during social situations (Schultz and Heimberg, 2008), which main- u
e
vestigate changes in the neural bases of emotion regulation in a ran- tains social anxiety symptoms by interfering with natural habituation st o
domizedcontrolledtrial(RCT)ofMBSRandaerobicexercise(AE)for processesthatleadtocorrectivelearning(HeimbergandBecker,2002). n 2
adults diagnosed withgeneralized socialanxiety disorder (SAD). Studies of patients with SAD have reported abnormal attentional 9 M
processes consisting of early hypervigilance followed by attentional a
Mechanisms underlying MBSR avoidance (i.e. reduced visual processing) of social threat (Mueller rch
MBSR is associated with decreases in the habitual tendency to emo- et al., 2008). Imaging studies with patients with SAD have begun to 201
identify specific neural patterns related to these abnormal attentional 9
tionallyreact toandruminate abouttransitorythoughts andphysical
processes. Findings include hyperactivity in brain regions related to
sensations(Teasdaleetal.,2000;Rameletal.,2004),stress,depression
immediate emotional reactivity (amygdala, insula) (Stein et al.,
andanxietysymptoms(Segaletal.,2002;Evansetal.,2008;Chiesaand
2007) and insufficient recruitment of brain networks implicated in
Serretti,2009)anddistortedself-view(Goldinetal.,2009c).MBSRis
cognitivereappraisal[dorsolateralprefrontalcortex(dlPFC),dorsome-
alsoassociatedwithincreasesinbehavioralself-regulation(Lykinsand
dial prefrontal cortex (dmPFC), dorsal anterior cingulate cortex
Baer, 2009), volitional orienting of attention (Jha et al., 2007) and
(dACC)] and attention regulation [posterior cingulate (PC)/precu-
emotion regulation (Goldin andGross, 2010; Modinos etal., 2010).
neus, inferior parietal lobe (IPL), supramarginal gyrus] when
Received12August2011;Accepted30April2012 modulatingresponsestosocialthreat(Goldinetal.,2009b)andnega-
AdvanceAccesspublication13May2012 tiveself-beliefs (Goldin etal., 2009a).
Theauthorsofthismanuscriptdonothaveanydirectorindirectconflictsofinterest,financialorpersonal Although effective cognitive–behavioral and pharmacological treat-
relationshipsoraffiliationstodisclose.ThisworkwassupportedbytheNationalCenterforComplimentaryand
ments have been developed for adults (Heimberg and Becker, 2002),
AlternativeMedicineInstitutesofHealthawardedtoJamesGross[GrantAT003644].
investigating alternative approaches to help 30–40% of the patients
CorrespondenceshouldbeaddressedtoPhilippeGoldin,DepartmentofPsychology,JordanHall,Bldg.420,
Stanford,CA94305-2130,USA,E-mail:[email protected] who do not respond to traditional interventions is warranted
(cid:2)TheAuthor(2012).PublishedbyOxfordUniversityPress.ForPermissions,pleaseemail:[email protected]
66 SCAN(2013) P.Goldinetal.
(SteinandStein,2008).PreliminaryevidencesuggeststhatMBSRmay specific phobia. Participants were excluded if they had previously
be helpful for patients with SAD. MBSR has been found to improve completedanMBSRcourseoriftheyhadaregularmeditationpractice
mood,functionalityandqualityoflifeinpatientswithSAD(Koszycki or AE regime (defined for our purposes as three or more times per
et al., 2007). MBSR-related changes in self-referential processing and week, for >2 months).
attention regulation have also been observed in patients with SAD InMBSRparticipants, currentAxisIcomorbidity included 10with
(Goldin et al., 2009c; Goldin and Gross, 2010). More specifically, generalizedanxietydisorder,5withmajordepressivedisorder,3with
during attention regulation, increased recruitment of posterior (par- specificphobia,2withdysthymia,2withpanicdisorder,1withagora-
ietalandoccipital)corticalattention-relatedbrainregionsfrompre-to phobia and 1 with obsessive–compulsive disorder. Past Axis I
post-MBSR was related to decreased anxiety in patients with SAD comorbidity included nine with major depressive disorder, three
(Goldin and Gross, 2010). While these initial studies are promising, witheatingdisorders,onewithpanicdisorderandonewithdysthymia.
little is known about how MBSR impacts emotion regulation, how it Fifteen participants reported past, non-cognitive–behavioral psycho-
influencestheneuralbasesofemotionregulationandhowitcompares therapy and sevenreported pastpharmacotherapy.
in the context of an RCT to other alternative and effective interven- In AE participants, current Axis I comorbidity included eight with
D
tions that havebeen shown toreduce stress andanxiety suchasAE. generalizedanxietydisorder,sixwithmajordepressivedisorder,three o
w
withdysthymia,twowithspecificphobia,twowithpanicdisorderand n
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The present study two with agoraphobia, Past Axis I comorbidity included two with ad
TofheMgBoSaRlovfsthAeEp(raensenatltestrundaytivweassttroessinrveedstuicgtaitoenthinetderifvfeenretniotnia)leinffetchtes mdisaojorrdedre,p1rewssiitvhe doibssoersdsievre,–ocnoemwpiutlhsivsuebdstiasonrcdeearbaunsed, oonneewwiitthhepaatinnigc ed fro
m
contextofanRCTontheneuralbasesofemotionregulationofnega- disorder. Nine participants reported past, non-cognitive behavioral h
tive self-beliefs in patients with generalized SAD. To do this, we ob- psychotherapy and five reported pastpharmacotherapy. ttp
s
tained behavioral and neural measures of emotion regulation during ://a
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anfMRIexperimentinpatientswithgeneralizedSADatbaselineand Procedure a
d
again after beingrandomly assigned to MBSRor AE. Allparticipantswererecruitedthroughweb-basedcommunitylistings em
WechoseAEasanalternativeinterventionforseveralreasons.Like and referrals from mental health providers. Participants were told on ic.o
MBSR,AEhasbeenshowntoimprovebothphysicalandmentalhealth the phone that the study involved random assignment to two stress up
(Penedo and Dahn, 2005), especially symptoms of stress, depression reduction programs. After passing a telephone screening, potential .co
and anxiety (Petruzzello et al., 1991; Stich, 1998; Stro¨hle, 2009) in participants were administered the ADIS-IV-L (Di Nardo et al., m/s
clinicalsamplesofmixedanxiety(e.g.Merometal.,2007),panicdis- 1994) by a clinical psychologist (P.G. or M.Z.). We enrolled patients ca
order(e.g.Broocksetal.,1998;Dratcu,2001)andgeneralizedanxiety with a principal diagnosis of generalized SAD (operationalized as n/a
disorder(e.g.Steptoeetal.,1989;McEnteeandHalgin,1999).Similar moderate or higher severity ((cid:2)4 on a scale of 0–8) on the rtic
to MBSR, it is a low-cost intervention that is readily available in the ADIS-IV-L (i) Clinician’s Severity Rating for SAD and (ii) social fear le-a
community. Furthermore, as implemented in this study, individual for five or more distinct social or performance situations in the SAD bs
and group practice for both MBSR and AE were easy to match and section.Allparticipantsprovidedinformedconsentinaccordancewith tra
c
control.InpatientswithSAD,theeffectsofAEontheneuralbasesof Stanford University Human Subjects Committee rules. t/8
emotionregulationhavenotbeenexaminedorcomparedtoMBSRin Participantswererandomly assigned to 8weeks ofeitherMBSR or /1/6
anRCT. AEusingEfron’sbiasedcoinrandomizationprocedure(Efron,1971), 5/1
Compared to AE, we expected MBSR to be associated with greater whichentailshigherprobabilityofallocationtotheunder-represented 69
(i) reduction of negative emotion and (ii) recruitment of posterior treatment group throughout the duration of the clinical trial. 47
8
cortical attention-related brain regions during attention regulation. Randomizationwasdoneonlyafterallbaselineassessments(including 4 b
IntheMBSRgroup,weexpectedmeditationpracticetobeassociated fMRI) werecompleted. y g
with decreased negative emotion and increased brain responses in Participants were administered self-report clinical and well-being ue
attention-related posterior cortical regions from baseline to measures (Jazaieri et al., 2012) and fMRI scanning assessments st o
post-MBSR. before andafter MBSR andAE. n 2
9
M
METHODS a
Interventions rc
Participants Mindfulness-based stress reduction h 2
0
Participants were patients seeking treatment for SAD and who met 1
We administered the standard MBSR program consisting of eight, 9
DSM-IV (Association, 1994) criteria for primary generalized SAD
weekly 2.5h group classes, a 1-day meditation retreat and daily
based on the Anxiety Disorders Interview Schedule for the
home practice. Participants were trained in formal meditation (i.e.
DSM-IV-Lifetime version (DiNardo et al., 1994). Of the 316 individ-
breath-focus, body scan, open monitoring), informal practice and
ualsassessedforeligibility,260wereexcludedduetonotmeetingstudy
Hatha yoga. Daily logs were collected each week to measure group
criteria (173), other reasons (66) or declined to participate (21). The
and individual meditation and yoga practice. Participants attended
remaining 56 participants were randomly assigned to either MBSR
MBSR courses offered by seven different teachers in eight health care
(n¼31) or AE (n¼25) (Figure 1). Groups did not differ in gender,
settingsthroughouttheSanFranciscoBayArea.MBSRinstructorshad
age, ethnicity or education (Table 1). Complete fMRI assessments at
15.7 years (SD¼4.1 years, range¼10–20 years) of MBSR teaching
both baseline and post-intervention were available for 23 MBSR and
experience. MBSRwasoffered atno-cost.
19AEparticipants.
ParticipantspassedanMRIsafety screenandwereexcludedifthey
had current pharmacotherapy or psychotherapy, history of medical Aerobic exercise
disorders or head trauma, or current psychiatric disorders other than We provided at no cost 2-month gym memberships to participants
SAD,generalizedanxietydisorder,majordepressivedisorder,obsessive randomizedtoAE.Tomatchtheindividualandgroupcomponentsof
compulsivedisorder,agoraphobiawithoutahistoryofpanicattacksor MSBR,participantsintheAEinterventionwererequiredtocomplete
MBSRvsAEinsocialanxiety SCAN(2013) 67
Assessed for eligibility (n=316)
Excluded (n=260)
♦ Not meeting inclusion criteria (n=173)
♦ Other reasons (n=66)
♦ Declined to participate (n=21)
Enrollment
Randomized (n=56)
• 31 MBSR
• 25 AE
D
Allocation ow
n
lo
a
d
e
Allocated to MBSR intervention (n=31) Allocated to AE intervention (n=25) d
♦Received intervention (n=26) ♦Received intervention (n=23) fro
m
♦Did not receive allocated intervention (n=5) ♦Did not receive allocated intervention (n=2) h
Reasons: 1 attended 4 classes and was Reasons: 1 wanted to but too anxious to get to ttp
s
uclnacsosemsf aonrtda bthleo uwgihtht gthroe ucpla fsosr, m1 aatt twenasd etodo 2 gity wma,s 1 t ocoo ufladr nawota fyind time to get to the gym as ://ac
intense, 1 attended 1 class and did not like the ad
content, 1 attended 0 classes and wanted to do em
something else for treatment, 1 attended 0 ic
classes because could no longer make class .ou
time p.c
o
m
/s
Follow-Up c
a
n
♦ Lost to follow-up (n=3) ♦ Lost to follow-up (n=4) /a
Reasons: 1 too busy, 1 could not complete Reasons: 1 too busy, 1 could not complete rtic
assessments in allotted time, 1 not willing to assessments in allotted time, 1 not willing to le-a
do fMRI again complete, 1 no response b
s
tra
c
t/8
/1
Analysis /6
5
Analyzed (n=23) Analyzed (n=19) /1
6
♦Excluded from analysis (n=0) ♦Excluded from analysis (n=0) 94
7
8
4
b
Fig.1 Consolidatedstandardsofreportingtrials(CONSORTs)diagramforaRCTofMBSRvsAE. y
g
u
e
s
t o
at least two individual AE sessions and one group AE session (other Fivesituationswerepresentedinasinglerunlasting15minand27s. n 2
than meditation oryoga) each week during the8-week intervention. Thesequenceofinstructionsforthefivesituationswasfixed:neutral, 9 M
reactNSB, regulateNSB, reactNSB andregulate NSB.Eachsituation a
rc
Experimental task consistedof(i)aninstructionto‘react’ or‘observe’(6s),(ii)16sen- h 2
tences (3s each) in white font against a black background describing 0
A version of this task focused on cognitive reappraisal has been pub- 1
thesituation,(iii)10NSBs(9seach)embeddedintheunfoldingstory 9
lished (Goldin et al., 2009a). The version used here implemented a
inuppercaselettersthatflashedninetimes(850msonand150msoff)
meta-cognitiveattentionregulationcuedwithasingleword‘observe’.
The task consisted of five situations. The first was an and(iv)anegativeemotionratingaftereachNSB(3s)from1¼notat
experimenter-composed neutral situation about washing a car that all to 3¼moderately to 5¼extremely negative (Figure 2). Negative
was used to obtain baseline emotion ratings and fMRI BOLD signals self-beliefs were flashed to maintain attention and appeared in white
forreadingneutralstatements.Then,fourparticipant-generatedauto- font for neutral and react trials and green for reappraisal trials. The
biographical social anxiety situations characterized by social anxiety, taskwasprogrammedinEprime(PsychologySoftwareTools,Inc)with
humiliation and embarrassment were presented. For each situation, abuttonresponsepadpositionedintheparticipant’srighthandinside
participants composed a paragraph describing the events, thoughts themagnet.Participantsweretrainedpriortothebaselinescantoreact
and feelings and five negative self-beliefs (NSBs) (e.g. I am incompe- toNSBsbyreflectingonhowtheNSBrepresentssomethingthatistrue
tent;othersthinkIamnotnormal).Participantsindicatedtheirageat about the participant. Observing NSBs consisted of cultivating a pre-
thetimeofeachsituationandprovidedratings,onascalesof1(notat sent moment, meta-cognitive attentional perspective that focused on
all)to9(verymuch),ofthevividnessofthememory,theirexperience just noticing any thought, memory, emotion or sensation as it ap-
of shame at the time of the situation, as well as current shame, pearedanddissolvedofitsownaccordwithoutgraspingatorrejecting
disturbance, avoidance andfrequency oftalking about thesituation. anyexperience ofbodyor mind.
68 SCAN(2013) P.Goldinetal.
Table 1 Demographic characteristics for patients randomizedto MBSRorAE Instruction: REACT or OBSERVE
S1-3
MBSRn¼31 AEn¼25 t-testor(cid:2)2 NSB1 S = Sentence = 3s each
S4-5
Females,n(%) 19(61.3) 10(40) (cid:2)2¼2.88 NSBS26 NSB = 9s Negative Self-Belief +
Age(M(cid:4)SD)(years) 32.87(cid:4)8.83 32.88(cid:4)7.97 t¼0.42 NSB3 3s Negative Emotion Rating
Ethnicity,n(%) (cid:2)2¼0.43 S7-8
NSB4
Caucasian 13(41.9) 10(40) S9-10
Asian 14(45.2) 11(44) NSB5
Hispanic 3(9.7) 1(4) S11-12
NSB6
Multiracial 1(3.2) 3(12) S13
Education(M(cid:4)SD)(years) 16.40(cid:4)2.00 16.84(cid:4)2.64 t¼0.34 NSB7
Currentaxis-Icomorbidity (cid:2)2¼0.88 S14NSB8
Generalizedanxietydisorder 10 8 S15
Majordepressivedisorder 5 6 NSB9
Dysthymia 2 3 S16
NSB10 D
Specificphobia 3 2 o
w
Panicdisorder 2 2 n
Agoraphobia 1 2 Fig.2 Structureofoneautobiographicalsocialsituationblockwith10trialsembedded. lo
a
Obsessive–compulsivedisorder 1 0 de
PasMtaajxoisr-Idecpormesosribviedidtyisorder 9 2 (cid:2)2¼1.49 convolvedwiththegammavariatemodel(Cohen,1997)ofthehemo- d fro
m
Dysthymia 1 0 dynamicresponsefunction.FunctionalMRIBOLDsignalintensitywas h
Panicdisorder 1 0 computed as percentage of signal change [(MR signal per voxel per ttp
Obsessive–compulsivedisorder 0 1 s
Substanceabuse 0 1 time point/mean MR signal in that voxel for the entire functional ://a
Eatingdisorder 3 1 run)(cid:3)100]. ca
Pastpsychotherapy 15 9 (cid:2)2¼1.84 Individual brain maps were converted to Talairach atlas space de
Pastpharmacotherapy 7 5 (cid:2)2¼1.56 (Talairach and Tournoux, 1988) and second-level group statistical mic
parametric maps were produced according to a random-effects .o
Note.MBSR¼Mindfulness-BasedStressReduction,AE¼aerobicexercise. u
model. To investigate interaction effects, a 2 Group (MBSR, AE)(cid:3)2 p.c
Time (pre, post) repeated-measures ANOVA (3dANOVA3 in AFNI) om
was implemented for regulate vs react NSBs. Follow-up t-tests /s
c
a
examined within- and between-group effects. n
Image acquisition /a
ImagingwasperformedonaGeneralElectric3-TSignamagnetwitha Tocorrectformultiplecomparisons,weused3dFWHMxtocalcu- rtic
late the intrinsic smoothness of the noise (i.e. residual in the BOLD le
T2*-weighted gradient echo spiral-in/out pulse sequence (Glover and signaltimeseries)foreachsubject.Wethencomputedthegroupmean -a
b
Lhmaeiawndi,m-2co0iz0iel1d()GuaEsnidHngeaaalctuhbscittaoer-meb,a-Mbruialinwltdaqufukoaeadem,raWtpuaIr,deUd‘iSdnAogm)..AeH’cereaolldsispmtaiocsavilenmbgilerednftucwnagace-s oFmWraigtHtineMralm(sa5izs.k4e4gv1eo5nx1ee)rlasatne(dd3.4be4nyt(cid:3)3edr3eA.d4u4ttho(cid:3)ims4av.s5aklmu.eFmoi)nrtaaorve3odxrCeeqll-uuwsiitrsSeedimPt¼owi0at.ch0h0ai4evg,er7a.0ya stract/8/1
tional run, 618 functional volumes were obtained from 22 sequential cluster-wise P-valueofP¼0.05. /6
5
axial slices (repetition time¼1500ms, echo time¼30ms, flip To examine the association of practice (meditation in MBSR and /1
6
angle¼608,fieldofview¼22cm,matrix¼64(cid:3)64,single-shot,reso- exercise in AE) and whole-brain BOLD responses for the contrast of 94
lution¼3.438mm2(cid:3)4.5mm; voxel volume¼53.2 mm3). 3D regulatevsreactNSB,weusedAFNI3dRegAnawiththesamethresh- 78
4
high-resolution anatomical scans were acquired using fast spin-echo olding procedure noted above. b
spoiled gradient recall (0.85942(cid:3)1.5mm; field of view¼22cm, y g
u
frequency encoding¼256). e
RESULTS s
t o
Preliminary analyses n
fMRI data preprocessing Ofthe31participants,5(16%)droppedfromMSBR,andofthe25,2 29 M
Analysis of functional neuroimages (AFNI) software (Cox, 1996) was (8%)participantsdroppedduringAE,anon-significantdifference,(cid:2)2 a
usedforpreprocessingandstatisticalanalysis.Thefunctionalrunwas (1, N¼56)¼0.84, P¼0.36. Between-group t-tests showed that the rch
subjectedtopreprocessingstepstomaximizesignal-to-noisecontrast. average amount of practice time each week in the MBSR (M¼212, 20
1
Thisincludedananalysisofpotentialoutliers,volumeregistrationtoa SD¼104min) and AE (M¼196, SD¼86min) groups did not differ 9
base image, motion correction, 4mm3 isotropic Gaussian spatial [t(45)¼0.60, P>0.55].
smoothing, masking non-brain voxels, high-pass filtering (.011Hz), Below,wereportthedifferentialeffectsofMBSRvsAEonnegative
linear detrending and conversion into BOLD signal percentage emotionratingsandneuralresponseswhenreactingtoandregulating
change in each voxel. No volumes demonstrated motion in the x, y negative self-beliefs. Within MBSR and AE groups, separately, we
or z directions in excess of (cid:4)0.8mm. There was no evidence of report the association of practice (meditation or AE) with negative
stimulus-correlated motion, as assessed by correlations between emotion ratings during emotion regulation and with thresholded
condition-specific reference functions and x, y, z motion correction whole-brain responses for the contrast of regulate vs react NSBs. The
parameters (allP’s>0.48). effectsofMBSRandAEonclinicalandwell-beingmeasuresinpatients
withSAD is reported elsewhere(Jazaieri etal., 2012).
fMRI statistical analysis
Emotional reactivity
Multiple-regression was implemented with AFNI 3dDeconvolve and
included baseline parameters to remove mean, linear and quadratic Negative emotion
trends and motion-related variance in the BOLD signal. Regressors A 2 Group (MBSR, AE)(cid:3)2 Time (baseline, post) repeated-measures
for the react NSBs, regulate NSBs and read neutral statements were ANOVA for the negative emotion ratings yielded no interaction of
MBSRvsAEinsocialanxiety SCAN(2013) 69
group by time for negative emotion when reacting to NSBs Emotion regulation
[F(2,37)¼1.24, P>0.27]. There was a main effect of time Negative emotion
[F(2,37)¼24.48, P<0.001, partial (cid:3)2 ((cid:3)2) ¼0.40] and no effect of
p ToassesstheeffectofMBSRvsAEonemotionregulationofNSBs,we
group [F(2,37)¼0.80, P¼0.38] (Figure 3). To rule out story effects, conducted 2 Group (MBSR, AE)(cid:3)2 Time (baseline, post)
apairedt-testshowedthattherewerenodifferentialnegativeemotion
repeated-measuresANOVAonpercentreductionofnegativeemotion
responsestoNSBsinall56participantsduringbaselinereactsituation whenregulatingNSBs.Thisanalysisyieldedaninteractionofgroupby
1vs 2 [t(55)¼1.45, P¼0.15]. time [F(2,37)¼4.99, P¼0.03, (cid:3)2 ¼0.12], a main effect of group
p
[F(1,37)¼4.10, P¼0.05, (cid:3)2 ¼0.10] and no effect of time (P>0.25).
p
Follow-upt-testsrevealedasignificantincreaseinpercentreductionof
Neural responses negative emotion from baseline to post-training for MBSR
A 2 Group (MBSR, AE)(cid:3)2 Time (baseline, post) repeated-measures [t(20)¼2.13, P<0.05, (cid:3)2 ¼0.19], but not AE [t(17)¼0.98, P>0.34]
p
ANOVAonBOLDresponsesforthecontrastofreactNSBsvsneutral (Figure 3).To ruleoutstory effects, apaired t-test showed that there
statements resulted in interactions of group by time in one region: were no differential negative emotion responses to NSBs in all 56 D
right ventrolateral PFC (Table 2). This effect was characterized by participants during baseline regulate situation 1 vs 2 [t(55)¼0.89, ow
n
baseline to post-intervention BOLD response decrease for MBSR [% P¼0.37]. lo
a
BOLDchange¼(cid:5)0.07%;t(22)¼2.90,P¼0.008]andincreaseforAE AmongMBSRparticipants,totalmeditationpracticewasassociated de
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sponses withonly one braindissociation intheprefrontal cortex. AreEdupcatriotincipoafnntes,gathtievreeewmaostnioonadssuorciniagtieomnootfioAnErepgruaclatitcioenw(itPh>p0e.r6c9e)n.t http
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4.0 Neut React Regulate AAN2OGVrAouopn(wMhBoSleR-,bAraEin)(cid:3)BO2LTDimrees(pboansseelisnfeo,rptohset)corenpteraastetdo-fmreeagsuularetes ic.ou
N 3.5 vpserrieoarctpNarSieBtsalyileolbduedlef(ivSePLsi)g,ntiwficoanrtegiinotnersacwtiiothnisn, itnhcelurdiginhgt rIiPgLh,t lseuf-t p.com
O
I lingual gyrus and cerebellar culmen (Table 2 and Figure 5). /s
OT 3.0 Follow-up t-tests in these interaction brain regions revealed baseline can
M /a
E E 2.5 to post-MBSR BOLD response decreases in right posterior superior rtic
V temporal gyrus (STG), and bilateral lingual gyrus, and increases in le
ATI 2.0 left IPL, right anterior IPL, right posterior IPL and right SPL. From -abs
EG baselinetopost-AE,pairedt-testsshowedBOLDresponsedecreasesin tra
N 1.5 right SPLand bilateral IPLand increases inright lingual gyrus. ct/8
AmongMBSRparticipants,totalamountofmeditationpracticewas /1
1.0 MBSR MBSR AE AE NasSsoBcsi)ataefdterwiMthBSinRcrteraasiendinBgOinLDMrPeFspCo,nlseefts IdPuLr,inlgeftremguidladtlee(ovcscirpeiatcatl /65/16
9
BASELINE POST BASELINE POST gyrus)(Table3).Therewerenoassociationsbetweenmeditationprac- 4
7
tice and react (vs regulate NSBs). Among AE participants, there were 8
4
Fig.3 TheeffectofMBSRandAEonnegativeemotionratingswhenreadingneutralstatements, noassociationsbetweenamountofAEandBOLDresponsesforregu- b
trheaectminegana.ndregulatingnegativeself-beliefs.*P<0.05,**P<0.005.Errorbars¼standarderrorof latevs react NSBs or reactvs regulate NSBs (allP’s>0.10). y gu
e
s
t o
DISCUSSION n
2
Table2 BOLDResponsesforinteractionofGroup(MBSR,AE)(cid:3)Time(pre,post)forreact 9
Thegoalofthisstudywastoinvestigatehowmindfulnessmeditation M
negativeself-beliefsvsreadneutralstatementsandregulatevsreactnegativeself-beliefs
andAEstressreduction training programs differentially influence be- a
rc
Brainregions(Cluster#) BA xa ya za Vol(mm3) F-value havioral and neural outcomes in the context of emotion regulation. h 2
0
1
9
ReactNSBs>readneutral
Rventrolateralprefrontalcortex 10 21 45 5 529 15.8 0
Readneutral>reactNSBs none N
Regulate>reactNSBs O -5
Parietallobes ON OTI -10
RSPL3 7 24 (cid:5)72 53 426 8.2 TIM
RIPL2 40 52 (cid:5)58 50 479 10.5 CE -15
RIPL5 40 58 (cid:5)41 46 372 13.7 DUVE -20
OccLipliitnaglulaolbegsyrus4 18 (cid:5)21 (cid:5)68 (cid:5)2 372 9.3 % REGATI -25 *
Cerebellum E -30
Culmen1 0 (cid:5)37 (cid:5)9 745 8.0 N
-35
React>regulateNSBs none
MBSR MBSR AE AE
aTalairachcoordinatesforvoxelwithpeakBOLD%signalchange. BASELINE POST BASELINE POST
F(cid:2)7.66, voxel P<0.004, minimum cluster volume threshold (cid:2)372mm3 (7 vox-
els(cid:3)3.438mm2(cid:3)4.5mm),cluster-wiseP<0.05. Fig.4 Percentreductioninnegativeemotionduringemotionregulationofnegativeself-beliefsat
BA¼Brodmann Area, BOLD¼blood oxygen dependent, L¼left, NSBs¼negative self-beliefs, baselineandpost-MBSRandAE.InteractionofGroupbyTime:F(2,37)¼4.99,P¼0.03,(cid:3)2¼0.12.
p
R¼right,Vol¼volume.TheCluster#aftereachbrainregionreferstoFigure5. Errorbars¼standarderrorofthemean.*P<0.05
70 SCAN(2013) P.Goldinetal.
5
3
1 4 2
000000000000000000000000000000000000000000.................1111111111111111111111111111111111888888888888888888888888888
z=-9 z=-3 z=45 z=52
0.15
MBSR AE
0.12
0.09
D
E 0.06 o
G w
N n
A 0.03 lo
H a
L C 0 ded
GNA -0.03 from
% SI -0.06 http
s
-0.09 ://a
c
a
-0.12 d
e
m
-0.15 ic
.o
1 2 3 4 5 u
-0.18 p
.c
o
m
Fig.5 BOLDresponsesforinteractionofGroup(MBSR,AE)(cid:3)Time(Pre,Post)forregulatevsreactnegativeself-beliefscontrast.Percentsignalchange¼ChangeinBOLDsignalfrompre-topost-intervention.
/s
InteractionofGroupbyTime:F(2,40)(cid:2)7.66,P¼0.004,Errorbars¼standarderrorofthemean.1¼Culmen,2¼RightIPL,3¼RightSPL,4¼LeftLingualGyrus,5¼RightIPL. c
a
n
/a
rtic
Table3 Associationbetweentotalamountofmeditationandwhole-brainBOLDsignal post-interventionBOLDsignaldecreaseforMBSRandincreaseforAE. le-a
forobserve vsreact NSBsatpost-MBSR in23 patients withSAD Right ventrolateral PFC has been implicated in cognitive control bs
processes including cognitive reappraisal of emotion (Ochsner and tra
Brainregions BA xyza Vol(mm3) t-value R2 Gross, 2005), response inhibition (Aron et al., 2004) and expressive ct/8
Observe>react suppression(Goldinetal.,2008).Thispatternofbrainactivitychanges /1/6
Frontallobes may be related to lesser automatic cognitive control of emotion 5/1
Lmedialprefrontalcortex 6 (cid:5)10(cid:5)1050 729 3.95 0.43 experience whilereacting toNSBs inMBSR. 69
Parietallobes 4
7
LIPL 40 (cid:5)52(cid:5)3739 1000 4.89 0.53 8
4
Occipitallobes Emotion regulation b
y
LMiddleoccipitalgyrus 19/31 (cid:5)28(cid:5)6822 891 4.10 0.44 MBSR, but not AE, resulted in a significant reduction in negative g
React>observe–none emotiontoNSBswhenimplementingtheattentionalemotionregula- ues
aTalairachcoordinatesforvoxelwithpeakt-value. tion strategy deployed in the experimental task. This converges with t on
t-value threshold(cid:2)3.14, voxel P<0.005, minimum cluster volume threshold(cid:2)372mm3 (7 prior findings of MBSR-related reduction in negative emotion when 2
Tvooxuernlso(cid:3)ux4c.o5omrdmin(cid:3)ate3s.,43R82¼mvma2r)ia,nccleusetexrplaPin<ed0..05. BA¼Brodmann area, x, y, z¼Talairach and implementingbreath-focusedattentionregulationofNSBsinpatients 9 M
a
withSAD(GoldinandGross,2010).Theattentionregulationstrategy rc
h
used here is a meta-cognitive attentional focus referred to as ‘open 2
0
monitoring’ or ‘receptive awareness’ in various contemplative trad- 1
9
Thetargetwaspresentmomentfocusedmeta-cognitiveattentionregu- itions. The degree of reduction in negative emotional reactivity with
lationinpatientswithgeneralizedSADwhentheyinteractedwiththeir attentional emotion regulation at post-MBSR is similar to what has
own negative self-beliefs embedded in autobiographical social anxiety been reported during cognitive reappraisal of NSBs in patients with
relatedsituations. SAD (Goldin et al., 2009a). This suggests that distinct emotion regu-
lation strategies areeffective in patients withSAD.
Practice dose effects were observed for MBSR, but not AE.
Emotional reactivity Meditation practice during MBSR was associated with lesser negative
MBSRand AEresulted in equivalent reduction of self-reported nega- emotionduringregulationofNSBs.Thesetofmindfulnessmeditation
tive emotional reactivity to NSBs. This converges with a prior study skillstaughtinMBSRmayimpactcorefeaturesofSAD,namely,social
showing MBSR-related reduction in negative emotional reactivity to fear, behavioral avoidance and exaggerated emotional reactivity by
NSBsinpatientswithSAD(GoldinandGross,2010).Thisisthefirst promoting a more flexible and adaptive attentional engagement with
studytodemonstratethatAEreducesemotionalreactivitytoNSBsin corenegativeself-beliefs.Thisislikelyaresultoftheextensivetraining
patients withSAD. in recognizing habitual patterns of thinking and interpreting in con-
The contrast of react NSBs vs read neutral statements yielded an junction with flexible implementation of meta-cognitive attention
interactionintherightventrolateralPFC,characterizedbybaselineto regulation. The absence of a practice effect in the AE group suggests
MBSRvsAEinsocialanxiety SCAN(2013) 71
that improvement in clinical and well-being measures with AE in WhilethisstudyinvestigatedbrainchangesbeforeandafterMBSR,
patientswithSAD(Jazaierietal.,2012)islikelyrelatedtomechanisms to address the issue of optimal treatment matching, future analyses
other than meta-cognitive attention regulation, such as reduction in should determine if behavioral and neural signals during emotion
autonomicreactivityoranxietysensitivity.However,thishasyettobe regulation at baseline can predict who will maximally benefit from
investigated inthecontext ofSAD. MBSR or AE (i.e. moderator analysis). To better understand how
BrainresponsesfromthecontrastofregulatevsreactNSBsprovide MBSR and AE work, an analysis of underlying mechanisms might
evidence for the role of posterior parietal attention-related brain investigate whether changes in BOLD responses from baseline to
regionsinelucidatinghowMBSRtrainsattentionprocessesinpatients post-intervention predict longer term clinical status (i.e. mediator
with SAD. The brain response interactions revealed a dissociation analysis). Specifically, future studies may consider investigating
characterized by MBSR increases and AE decreases in three posterior whetherandhowchangesinemotionregulationstrategyduringtreat-
parietal attention-related brain regions: right anterior IPL, right pos- mentare relatedto clinical outcomes.
teriorIPLandrightSPL.Thesebrainregionshavebeenimplicatedin
attentionalalertingtoastimulus(Fanetal.,2005).Enhancedrecruit-
FUNDING D
mentofthesebrainregionsfollowingMBSRmayreflectgreateratten- o
w
tional engagement (rather than avoidance or distraction) with the National Center for Complimentary and Alternative Medicine n
lo
emotionalprobe.MBSR-relatedincreasedactivationinsimilarparietal Institutesof Healthawarded to JamesGross [Grant AT003644]. a
d
cortex regions has been reported with breath-focused attention vs ed
distraction inpatients with SAD(Goldinand Gross, 2010). CONFLICT OF INTEREST from
theOrefwneortee,psriamctiilcaerdtoosteheeffpecattsteornnbwraitihnrseeslpf-orenpseosrtfeodrMneBgSaRti,vbeuetmnoottiAoEn,, Nonedeclared. http
s
specifically for the observe emotion regulation condition. Greater ://a
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