fear conditioning and extinction in anxious and nonanxious youth and adults

12 Pages·2017·0.47 MB·English

DEPRESSIONANDANXIETY32:277–288(2015)
Research Article
FEAR CONDITIONING AND EXTINCTION IN ANXIOUS
AND NONANXIOUS YOUTH AND ADULTS: EXAMINING
A NOVEL DEVELOPMENTALLY APPROPRIATE
FEAR-CONDITIONING TASK
TomerShechner,Ph.D.,1 JenniferC.Britton,Ph.D.,2 EmilyG.Ronkin,B.A.,3 JohannaM.Jarcho,Ph.D.,3
∗
JamieA.Mash,B.A.,3 KalinaJ.Michalska,Ph.D.,3 EllenLeibenluft,M.D.,4 andDanielS.Pine,M.D.3
Background: Fear conditioning and extinction have been implicated in the
pathogenesis of anxiety disorders. However, due to ethical and methodological
limitations, few studies have examined these learning processes across devel-
opment, particularly among anxious individuals. The present study examined
differencesinfearconditioningandextinctioninanxiousandnonanxiousyouth
and adults using a novel task designed to be more tolerable for children than
existing paradigms. Methods: Twenty-two anxious adults, 15 anxious youth,
30 healthy adults, and 17 healthy youth completed two discriminative fear-
conditioning tasks. A well-validated task paired a woman’s fearful face with
a scream as the unconditioned stimulus. The novel task paired a bell with an
aversive alarm as the unconditioned stimulus. Self-reported fear, skin conduc-
tance response, and fear-potentiated startle eye blink were measured. Results:
Bothtaskswerewelltoleratedandelicitedfearresponseswithmoderatestability.
Anxiousyouthandadultsreportedoverallgreaterfearthanhealthyparticipants
during the tasks, although no group differences occurred in discriminative fear
conditioningorextinction,asassessedbyself-reportorphysiology. Conclusion:
The novel bell-conditioning task is potent in eliciting fear responses but tol-
erable for pediatric and anxious populations. Our findings are consistent with
priorstudiesthathaveshowncomparablefearlearningprocessesinanxiousand
nonanxiousyouth,butdissimilarfromstudiesexhibitingbetween-groupdiffer-
ences in extinction. Given the limited research on fear conditioning in youth,
methodological issues and suggestions for future work are discussed. Depression
andAnxiety32:277–288,2015. C 2014WileyPeriodicals,Inc.
⃝
Key words: fear conditioning; extinction; pediatric anxiety; psychophysiology;
SCR;fear-potentiatedstartle
INTRODUCTION
C
onsiderable evidence suggests fear conditioning IsraelScienceFoundationISF-1377/14(TS);Contractgrantspon-
and extinction are fundamental to the expression of sor:NationalInstituteofMentalHealthR00-091183(JCB).
Allauthorsreportnoconflictofinterests.
1DepartmentofPsychology,UniversityofHaifa,Israel
2DepartmentofPsychology,UniversityofMiami,Florida ∗Correspondence to: Tomer Shechner, Psychology Department,
3SectiononDevelopmentandAffectiveNeuroscience,NIMH, UniversityofHaifa,MtCarmel,3498838,Haifa,Israel.
Bethesda,Maryland E-mail:[email protected]
4SectiononBipolarDisorder,NIMH,Bethesda,Maryland Received for publication 9 June 2014; Revised 17 August 2014;
Accepted3September2014
Contract grant sponsor: Intramural Research Program of the DOI10.1002/da.22318
National Institute of Mental Health, National Institutes of Health; Publishedonline27November2014inWileyOnlineLibrary
Contractgrantsponsor:MarieCurieCareerIntegrationGrantand (wileyonlinelibrary.com).
C 2014WileyPeriodicals,Inc.
⃝
278 Shechneretal.
anxietydisorders.Studyingfearconditioningandextinc- One neutral face, the CS , but not the other neutral
+
tionacrossdevelopmenthasgreatrelevanceforidentify- face, the CS , is paired with a fearful expression and
−
ingfactorsthatmoderateriskfor,andresilienceagainst, aversive auditory scream. Although potent in eliciting
pediatricanxiety.Themostcommonmethodforelicit- fear,thescreamingladytaskhastwomajorlimitations.
ing conditioned fear includes use of physically aversive First, similar to other studies in pediatric samples,[8,13]
unconditionedstimuli,suchaselectricalshock.Because a relatively high proportion of youth discontinued.
ethical constraints intrinsic to studying youth preclude Although no adults discontinued fear acquisition, 49%
theuseofphysicallyaversivestimuli,therearerelatively ofanxiousyouthand14%ofhealthyyouthdiscontinued
fewstudiesoffearconditioninginchildren.Onerecent due to high levels of fear.[1] Second, the use of social
study used a visual/audio pairing of a woman scream- stimuli as a CS could instantiate fear in subjects prone
ing as an unconditioned stimulus to compare condi- tosocialanxiety,evenintheabsenceoftheUCS.
tioned fear response in anxious and nonanxious youth The current study of anxious and healthy adults and
andadults.[1]Althoughtheresultsfromthisstudysuggest childrenutilizesanovelfear-conditioningparadigm,the
thepresenceofimportantdevelopmentaldifferencesin “belltask,”designedtoaddresstheselimitations.Inthis
fearconditioning,alargenumberofanxiouspatientsand task, two different color bells serve as CSs, and a red
youthabortedthetaskpriortocompletionbecausethey bell accompanied by an aversive alarm serves as the
foundthestimulitooaversive.Thisraisesconcernsabout UCS. Stronger conditioning and extinction occur on
the tolerability of the scream-based fear-conditioning tasks that use stronger, more potent, and biologically
task for anxious patients and younger age groups. The relevantstimuli.[3]Oneoftheconditioningparadigmsin
currentstudyexaminesdifferencesinfearconditioning thecurrentstudypairsaredbellwithanaversivealarm;
and extinction among anxious youth and adults using the other pairs a fearful face with an aversive scream.
the scream-based task and a novel paradigm developed Thus,bothpairsetsofpictorialandauditorystimulithat
toelicitfearwhileremainingtolerableforsensitivepop- also co-occur in genuinely dangerous situations in real
ulations. life. As such, these two paradigms may be more aver-
Modest evidence suggests that anxious adults are sivethanparadigmsusingonlyanauditoryUCS,possi-
more responsive to fear conditioning and extinction blybecausetheparadigmsevokereactionsthatoccurto
thanhealthyadults.However,thesedifferencesaremore aversiveeventsinchildren’sdailylives.
pronounced for single cue conditioning paradigms, Because the bell and screaming lady tasks share fea-
where one conditioned stimulus (CS) is paired with an tures, it is important to compare response to the two
unconditional stimulus (UCS), than for discrimination paradigms.Basedonpreviouswork,weexpectanxious,
conditioning paradigms, where one CS (CS ) but relativetononanxiousparticipants,toshowhigherlev-
not another CS (CS ) is paired with the U+CS.[2] elsoffeartobothCSs,butnodifferencesindifferential
−
Discrimination conditioning paradigms are imperative learningduringfearconditioningorextinction.Inorder
in the study of fear conditioning as they allow the tovalidatethenewtaskandexaminewithin-subjectcon-
examination of excitatory processes to danger cues sistency, each participant completed bell- and scream-
(CS ), inhibitory processes to safe cues (CS ), and based fear-conditioning and extinction paradigms. Re-
+ −
the ability to differentiate between the two stimuli. sultsfromthetwotasksarecomparedacrossanxietyand
Findings from the few discrimination-based condi- agegroups.
tioning studies that compare fear response in anxious
andnonanxiousyoutharesomewhatinconsistent(fora
reviewsee[3]).Somereportnogroupdifferencesinfear METHOD
conditioning,[1,4–6] whereas others report differences
PARTICIPANTS
in extinction.[4,6,7]. The most consistent findings are
Anxiousyouthsandadultsandtheirhealthycounterpartspartici-
that, regardless of age, anxious, relative to healthy
patedinthisstudyaspaidvolunteers.Writteninformedconsentfrom
individuals, exhibit elevated fear to both danger (CS )
+ adultparticipantsandparentsandwrittenassentfromyouthpartici-
andsafecues(CS ),butsimilarlevelsofdifferentialfear
learning.[1,4,5] − pantswereobtained.TheNationalInstituteofMentalHealthInsti-
tutionalReviewBoardapprovedallprocedures.
Conditioning paradigms in animals and adults Individuals were included in the study if they were medica-
typically employ an electric shock as the UCS, which tion free, physically healthy, and had an IQ > 70. All partici-
is generally considered to be inappropriate for use in pants received a comprehensive psychiatric assessment. The Struc-
pediatricpopulations.[8,9]Thus,moststudiesinchildren tured Clinical Interview for the DSM-IV-TR Axis I Disorders
haveusedmildlyaversivesoundsasaUCS,[8,10–12]which (SCID) was used for adults and the Kiddie Schedule for Affective
aremoretolerable,butelicitlowerlevelsofconditioned Disorders and Schizophrenia (KSADS) was used for children. Par-
ents and their children were interviewed separately. In line with
fear. To study fear conditioning across development,
previous clinical trials of anxiety disorders, child–parent discrep-
a more aversive UCS is needed to produce robust
ancies were resolved by the clinician as part of the diagnos-
conditioninginbothyouthandadults.The“screaming
tic process used in previous research-based assessment enrolling
ladytask”hasshownpromiseinthisrespect.[1,5,13,14] In children in treatment research.[15,16] Healthy youth and adults
thistask,participantspassivelyviewneutralfacesoftwo were included if they were free of any current Axis I disor-
women, which serve as the conditioned stimuli (CS). ders. Anxious youths and adults met DSM-IV-TR criteria for
DepressionandAnxiety
ResearchArticle:ExaminingaNovelDevelopmentallyAppropriateFear-ConditioningTask 279
a current anxiety disorder. Other comorbid anxiety disorders or ject’sleftforearm.EMGdatawereobtainedatasamplingrateof1,000
major depressive disorder were permitted, however current or Hzandfilteredusinganamplifierbandwidthof30–500Hz.
past diagnoses of PTSD or obsessive–compulsive disorder were
excluded.
PROCEDURES
Usingtheseprocedures,95participantsstartedthebelltask,but
three children aborted during conditioning, whereas 89 started the Twofear-conditioningtaskswerecompleted:thescreaminglady
screamingladytask,butthreechildrenabortedduringconditioning, taskandthenovelbelltask.Detailsonthescreamingladytaskwere
anddatafortwoadditionaladultparticipantswerelostduetotechni- describedpreviously(e.g.,[1]).Thebelltaskfollowsthesamecondi-
calmalfunction.Thus,84individualscompletedbothtasks.Noprior tioningproceduresasthescreamingladytask,butusesdistinctaudio
datahavebeenreportedfromeithertaskintheseparticipants,whichin- andvisualstimuli.Specifically,theCS andCS arepicturesofblue
+ −
cluded15anxiousyouths,22anxiousadults,17healthyyouths,and30 andyellowbells,insteadofpicturesoftwowomen’sfaces,andtheUCS
healthyadults.ClinicalanddemographicdataarepresentedinTable1. isanaversivebellsoundinsteadofascream.TheUCSconsistedof
Asexpected,self-reportandparent-reportSCARED(Self-Reportfor a1-simageofaredbellco-occurringwithanaversive95dBalarm
ChildhoodAnxietyRelatedEmotionalDisorder)scoreswerehigher (seeFig.1).Thesearecorollariesofthefearexpressionandscream
foranxiouscomparedtononanxiousyouth,t(30) 3.84,P<.001, usedasUCSinthescreamingladytask.Participantscompletedeach
=
t(29) 6.50,P<.001(respectively).Similarly,anxiousadultsreported task on a separate visit, with at least 3 days between the two visits
=
higheranxiety(indexedbyLiebowitzSocialAnxietyScalescores)than (Mdaysbetweentasks =25.64,SD=7.60).Theorderofthetwoproce-
theirnonanxiouscounterparts,t(53) 5.67,P<.001. dures(screamingladyorbelltask)wasrandomlydetermined.
=
Inbothtasks,thestimuliusedfortheCS andCS werecounter-
+ −
balancedacrossparticipants.TheCS andtheCS werepresented
+ −
for7–8sfollowedbyagrayscreen(intertrialinterval;ITI)presented
PSYCHOPHYSIOLOGICALDATAACQUISITION
for 8–21 s (averaging 15 s). The CS was followed by the UCS
+
Psychophysiologicalmeasureswereusedasoneindexoffearcon- accordingtoan80%reinforcementschedule.Airpuffs(4–10psiof
ditioning and extinction. Psychophysiological measures were col- compressedairfor40ms)weredeliveredtotheforeheadduringthe
lectedcontinuouslyusingPsyLabpsychophysiologicalrecordingsys- CS ,CS ,andITItomeasureFPS.Startleprobesweredelivered
+ −
tem(PsyLabSAMSystemContactPrecisionInstruments,London, 5–6safterCSonsettoallowformeasurementofSCRduringthefirst
www.psylab.com)duringtheprocedure. 5softhetrial.
Skinconductanceresponse(SCR)wasmeasuredwithtwoAg/AgCl The fear-conditioning tasks consisted of four different phases—
electrodesfilledwithnonsalinegelattachedtothemedialphalanxof habituation, preconditioning, fear conditioning, and extinction. In
themiddleandringfingersofthelefthand.[17]SCRdatawererecorded eachphase,theCS ,CS ,andITIwerepresentedindifferentblocked
+ −
usingasamplingrateof1,000Hz. counterbalancedorder.Beforethefirstphase,participantsweretold
Fear-potentiatedstartle(FPS)wasmeasuredwiththeeyeblinkstar- thattheymightseeunpleasantpictures,hearunpleasantsounds,and
tlereflexwithtwo6mmtin-cupelectromyography(EMG)electrodes feelanairpuffontheirforehead.Theywerealsotoldthatiftheypaid
filledwithstandardelectrolytesolutionplacedunderthesubject’sleft attentiontheymaylearntopredictwhenthesoundwilloccur,butthey
eyealongthecheekbone.Agroundelectrodewasplacedonthesub- werenotinformedoftheUCS/CS coupling.
+
TABLE1.Sampledemographics
Patients Healthy
Wholesample(n 84) Youths(n 15) Adults(n 22) Youths(n 17) Adults(n 30)
= = = = =
Subjectanxietydiagnosis
GAD 1 6
SoPh 4 4
SAD 1
GADandSoPh 2 9
GADandSAD 0
GADandPD 0 3
GADandSpecPh 2
SoPhandSAD 0
GAD,SoPh,andSAD 3
GAD,SoPh,andSpecPh 2
Anxietysymptomscores
Self-reportedSCAREDtotal 26.9(14.9) 7.7(5.6)
Parent-reportedSCAREDtotal 34.7(14.4) 4.8(5.4)
Self-reportedLSAStotal 58.5(25.1) 23.2(20.2)
Demographics
Meanage 11.5(2.57) 29.2(8.35) 13.0(2.97) 29.7(7.12)
No.offemales(percentageofsample) 7(46.7) 17(77.3) 9(52.9) 11(36.7)
TwoWASIsubscalesIQ 116.5(13.6) 114.9(11.2) 110.3(8.3) 116.6(12.8)
Note:GAD,generalizedanxietydisorder;SoPh,socialphobia;SAD,separationanxiety;PD,panicdisorder;SpecPh,specificphobia;SCARED,
Self-ReportforChildhoodAnxietyRelatedEmotionalDisorder;LSAS,Liebowitzsocialanxietyscale;PARS,PediatricAnxietyRatingScale;WASI,
WechslerAbbreviatedScaleofIntelligence.
TwoWASIsubscalesarevocabularyandmatrixreasoning.
DepressionandAnxiety
280 Shechneretal.
Figure1.Bell-conditioningtask.
During habituation, six startle probes without any visual stimuli tocontinue.Next,wepresenttheinterclasscorrelation
weredelivered.Inthepreconditioningphase,imagesoftheCS and analysis of the two tasks, which revealed correlations
+
theCS werepresentedfourtimeseach.Duringthefear-conditioning across tasks. Given these moderate to strong correla-
−
phase,imagesoftheCS andCS werepresented10timeseach.The tions, in a third analysis, fear responding was averaged
+ −
UCSwasdeliveredeighttimeswhilepairedwiththeCS+.Finally,in acrossthetaskstoincreasepowerinthisanalysis.There-
theextinctionphase,theCS andtheCS wereeachpresentedeight
+ − fore,thethirdanalysiscomparesanxiousandnonanxious
timesintheabsenceoftheUCS.
youthandadultsinfearconditioningandextinction,av-
Participants reported their levels of fear while viewing the CS
+ eragedacrossthetwotasks(Phase Stimuli Anxiety
andCS usinga10-pointLikertscale(1 non,10 extreme)dur- × ×
− = = group Age group). Finally, we present the complete
ingpreconditioning,andimmediatelyfollowingfearconditioningand
×
extinction. resultsfromthesix-wayomnibusANOVAsinthefourth
analysis.
DATAANALYSIS
Threedependentvariablesmeasureddifferencesinfearforprecon- DISCONTINUATIONOFTASKS
ditioning,conditioning,andextinctionphasesacrossthetwotasks:(1)
For the bell-conditioning task, two (10.5%) anxious
self-reportedfeartoeachbell/facefollowingeachphase;(2)average
children (one male and one female) and one (5.6%)
SCR level during each phase; (3)average EMGduring each phase.
nonanxiouschild(female)abortedduringfearcondition-
SCRforeachCS andCS wasdeterminedbythedifferencebe-
tweenbase-to-pea+kamplitud−ewithin5safterthestimulusonset.SCR ing.Forthescreamingladytask,one(6%)anxiouschild
scoreswerenormalizedusingasquare-roottransformation.EMGdata (male) and two (10.5%) nonanxious children (1 male
wererectifiedandsmoothedusingmovingaveragewith20mswin- and1female)abortedthetaskduringfearconditioning.
dows.Startleresponsedataforeachparticipantwasstandardizedusing Thus,discontinuationratesdidnotdifferacrossthetwo
aT-scoretransformation. tasksineithertheanxiousgroup,χ2 .203,P .653,
Interclass correlation coefficients were used to test for temporal (1) = =
orthenonanxiousgroup,χ2 .307,P .580.Partici-
stabilityofthethreedependentmeasuresacrossthetwotasks. (1) = =
Self-report and SCR measures were each submit- pantswhoterminatedonetaskwereexcludedfromthe
ted to a separate repeated measures ANOVA, with 2 analysis.
Tasks (bells, screaming lady) 3 Phases (preconditioning, Attrition rates among anxious and nonanxious youth
×
conditioning,extinction) 2Stimuli(CS ,CS )aswithin-subject alsowerecomparedtopreviousworkusingthescream-
× + −
factors×2Agegroups(youth,adults)×2Anxietygroups(anxious, ing lady task in pediatric samples (Britton, 2013 #958).
nonanxious) as between-subject factors. A third ANOVA was
Thus,ratesofdiscontinuationinindividualswhocom-
conductedforEMGforwhichthestimulifactorincludedthreelevels
pletedthescreamingladytaskfirstinthecurrentstudy
(CS , CS , ITI). Task order (first, second) was added as another
+ − werecomparedtoanxiousandnonanxiousyouthinthe
factor to each of these ANOVAs to examine for possible effects of
previous study.[1] Due to the small sample sizes, the
task order. Significant results for ANOVAs were further examined
forspecificeffectsusingposthocanalysis.Forallanalyses,statistical Fisherexacttestwasused.Comparedtosevennonanx-
significancewassettoα .05. iousof49whoabortedthetaskinthepreviousstudy,[1]
=
the current study found 1 of 10 nonanxious subject
abortedthescreamtaskwhenitwasdeliveredasthefirst-
RESULTS
conditioning task. The Fisher exact test statistics was
Foursetsofresultsarepresented.First,wereportthe notsignificant,P>.05.Thismeansthatattritionrates
numberofparticipantswhofoundthetaskstooaversive fornonanxioussampleswerenotdifferentacrossthetwo
DepressionandAnxiety
ResearchArticle:ExaminingaNovelDevelopmentallyAppropriateFear-ConditioningTask 281
TABLE2.Interclasscorrelations(ICC)coefficients[confidenceintervals]betweenthethreedependentvariablesacross
thetwotasks
Bell-conditioningtask
Conditioning Extinction
CS CS CS CS
+ − + −
Scream-conditioningtask Self-report Conditioning .62**[.41–.75] .45*[.16–.64]
Extinction .54**[.30–.70] .42*[.11–.62]
SCR Conditioning .65**[.46–.78] .63**[.42–.76]
Extinction .48*[.19–.66] .46*[.16–.65]
EMG Conditioning .36*[.01–.59] .34*[-.20–.56]
Extinction .02[-.59–.34] .26[ .14–.52]
− −
Note:∗∗P<.001;∗P<.05.Significantcorrelationsareindicatedinbold.
studiesforthescreamamongnonanxiousyouth.How- Stimuliinteractionwassignificantintheentiresample,
ever, compared to 22 of 45 anxious youth that aborted F(2,152) 21.38,P<.001,partialη2 .22(Table3),
thetaskinthepreviousstudy,[1]thecurrentstudyfound as well as=among anxious, F(2, 72) 1=1.36, P < .001,
alleightanxiouschildrensuccessfullycompletedit.The partial η2 .24 and nonanxious pa=rticipants, F(2, 92)
Fisher exact test statistics indicated a significant differ- 13.88,P=<.001,partialη2 .23(Fig.2A)considered
= =
ence between the studies, P < .05. Attrition rates were individually.Follow-upcontrastsrevealednodifferences
higherinthepreviousstudyamonganxiouschildren. between stimuli after preconditioning and significant
differences in self-reported fear to the CS compared
+
to the CS after fear conditioning and extinction in
ASSOCIATIONBETWEENTWOTASKS −
boththeanxiousandnonanxiousgroups(allPs<.001).
Interclasscorrelationanalysiswasconductedforeach
The ANOVA on self-reported fear with Phase-
dependentmeasure,separatelyforCS andCS ,across
+ − by-Stimuli-by-Anxiety group-by-Age group was not
the two tasks. As evident in Table 2, across all groups,
significant(Table3).
moderate to strong interclass correlation coefficients
werefoundduringconditioningandextinctionforself-
reported fear and SCR (ranging from .42 to .65), and SCR
modest correlation for EMG only during conditioning Likewise, several findings emerged when examining
(.34–.36)butnotextinction. SCRcollapsedacrosstasks.Themaineffectofagewas
significant,F(1,73) 24.28,P<.001,partialη2 .25,
= =
AVERAGERESPONDINGINANXIOUSAND indicatingoverallhigherlevelsofSCRinyouththanin
NONANXIOUSYOUTHANDADULTS adults. The main effect of stimuli was also significant,
COLLAPSEDACROSSTASKS F(1, 73) 8.17, P .006, partial η2 .10. SCR lev-
= = =
els were higher to the CS than to the CS . Results
ANOVAresultsforPhase Stimuli Anxietygroup + −
× × alsoindicatethatanxiousparticipantsdidnotdifferfrom
Agegroupaccordingtothethreedependentvariables
× nonanxiousparticipantsinfearconditioningandextinc-
(self-reported fear, SCR, EMG) collapsed across tasks
tion.
arepresentedinTable3.
The Phase-by-Stimuli interaction was significant in
the entire sample, F(2, 146) 8.48, P < .001, partial
SELF-REPORTEDFEAR η2 .10 (Table 3), as well a=s in the anxious, F(2, 64)
As shown in Table 3, several findings across tasks 5=.44, P .007, partial η2 .15, and nonanxious
emerged for self-reported fear. First, a main effect of =participants=,F(2,82) 3.36,P=.040,partialη2 .08,
anxietyemerged,F(1,76) 10.11,P .002,partialη2 considered individual=ly (Fig. 2B=). Follow-up con=trasts
= =
.12. Anxious participants reported higher levels of revealed a significant difference in SCR to the CS
= +
overallfearcomparedtotheirnonanxiouscounterparts. compared to the CS after fear conditioning (all Ps <
−
Second,themaineffectofphasewassignificant,F(2,152) .008), but not after preconditioning or extinction (all
71.32, P < .001, partial η2 .48. Participants re- Ps > .268). Yet differential learning was observed only
= =
ported higher levels of fear during conditioning than in youth but not in adults. A significant three-way in-
preconditioning (P < .001) and extinction (P < .001). teractionemergedforPhase-by-Stimuli-by-Agegroup,
Finally, the main effect of stimuli was significant, F(1, F(2, 146) 3.84, P .024, partial η2 .05 (Table 3).
76) 49.45, P < .001, partial η2 .39. Participants Examining=each age=group separately =yielded a signif-
= =
reportedhigherlevelsoffeartotheCS thantheCS . icant Phase-by-Stimuli interaction only in youth, F(2,
Both groups exhibited fear condit+ioning but n−ot 50) 5.59,P .006,partialη2 .18,butnotinadults,
extinction based on self-reported fear. The Phase F(2,=96) 1.9=2, P .153, part=ial η2 .04. Follow-up
× = = =
DepressionandAnxiety
282 Shechneretal.
TABLE3.ANOVAresultsforPhase Stimuli Anxiety Ageforthethreedependentvariables
× × ×
Self-report SCR EMG
Effect df F Significant df F Significant df F Significant
Effectsofconditioning
Phase 2,152 71.32** P<.001 2,146 1.92 P .151 2,148 105.33** P<.001
=
Stimuli 1,76 49.45** P<.001 1,73 8.17* P .006 2,148 66.87** P<.001
=
Phase Stimuli 2,152 21.38** P<.001 2,146 8.48* P<.001 4,296 4.36* P .002
× =
Effectsofage
Age 1,76 0.24 P .628 1,73 24.28* P<.001 1,74 4.89* P .030
= =
Phase Age 2,152 0.54 P .582 2,146 4.69* P .011 2,148 2.50 P .085
× = = =
Stimuli Age 1,76 0.00 P .985 1,73 5.95* P .017 2,148 0.36 P .699
× = = =
Phase Stimuli Age 2,152 0.20 P .820 2,146 3.84* P .024 4,296 0.58 P .676
× × = = =
Effectsofanxiety
Anxiety 1,76 10.11* P .002 1,73 0.43 P .515 1,74 0.18 P .671
= = =
Phase Anxiety 2,152 0.40 P .673 2,146 0.08 P .973 2,148 0.28 P .757
× = = =
Stimuli Anxiety 1,76 1.46 P .231 1,73 1.56 P .217 2,148 1.68 P .190
× = = =
Phase Stimuli Anxiety 2,152 0.56 P .571 2,146 0.70 P .501 4,296 0.46 P .764
× × = = =
Phase Stimuli Anxiety Age 2,152 1.06 P .350 2,146 1.37 P .256 4,296 0.72 P .583
× × × = = =
Note:SCR,skinconductanceresponse;EMG,electromyography;df,degreesoffreedom.
Significanteffectsareindicatedinbold.
contrasts revealed a significant difference between the TASK-SPECIFICRESPONDINGINANXIOUSAND
CS and the CS in youth (P .002) but not adults NONANXIOUSYOUTHANDADULTS
+ − =
(P .109). Tounderstandtaskdifferences,weconductedsix-way
=
The ANOVA on SCR with Phase-by-Stimuli- omnibusANOVAswith2Tasks(bells,screaminglady)
by-Anxiety group-by-Age group was not significant 3Phases(preconditioning,conditioning,extinction)
(Table3). ×2Stimuli(CS ,CS ) 2Agegroups(youth,adults)×
+ − × ×
2Anxietygroups(anxious,nonanxious) 2TaskOrder
×
FPS–EMG (belltaskfirst,screamingladytaskfirst)foreachofthe
dependentvariables(self-reportedfear,SCR,EMG).In
As with SCR, the main effect of age was significant,
F(1, 74) 4.89, P .030, partial η2 .18, with youth thenextsection,wepresenttheadditionaleffectsofTask
= = = andOrderandtheirinteractionswiththefourotherfac-
exhibiting higher overall levels of EMG compared to
torsreportedintheprevioussection(i.e.,Phase,Stimuli,
adults.Inaddition,amaineffectofphaseemerged,F(2,
148) 105.33, P < .001, partial η2 .59, indicating a Agegroup,andAnxietygroup).
= =
consistent habituation from preconditioning to condi-
tioning (P < .001)and fromconditioning toextinction SELF-REPORTEDFEAR
(P < .001). Finally, the main effect of stimuli was A main effect of Task emerged, F(1, 76) 9.34,
significant,F(2,148) 66.87,P<.001,partialη2 .48. P .003, partial η2 .11, with participants re=porting
= = = =
EMGlevelswerehighertotheCS thantotheCS . higherlevelsoffearfromthescreaminglady(M 3.00,
+ − =
As with the self-report and SCR data, the Phase-by- SD 0.17) than the bell-conditioning task (M 2.51,
= =
Stimuliinteractionwassignificantintheentiresample, SD 0.13).Thus,overall,reportedlevelsoffearinthe
F(4, 296) 4.36, P .002, partial η2 .06 (Table 3), curr=ent study were higher in the screaming lady task
= = =
as well as in the anxious, F(4, 144) 2.39, P .05, thaninthebell-conditioningtask.
η2 .06, and the nonanxious particip=ants, F(4, 1=76) The three-way interaction for Task-by-Phase-by-
2.4=6,P .047,η2 .05(Fig.2C).Follow-upcontras=ts Stimuli was significant, F(2, 152) 3.60, P .030,
revealed=a significa=nt difference in EMG to the CS partial η2 .045, with the bell ta=sk eliciting=greater
+ =
compared to the CS after fear conditioning (all Ps < differentiallearning(CS >CS )duringconditioning
− + −
.003), but not after preconditioning (all Ps > .418) or comparedwiththescreamingladytask.Thisdifference
extinction(allPs>.077). derives from higher level of reported fear to the CS
−
TheANOVAonEMGwithPhase Stimuli Anx- in the screaming lady task (M 3.30, SD 2.40)
× × = =
ietygroup Agegroupwasnotsignificant(Table3). comparedtotheCS inthebelltask(M 2.54,SD
× − = =
In sum, collapsed across the two tasks, both groups 2.00),t(83) 2.68,P .009inbothchildrenandadults.
= =
exhibitedfearconditioningandextinctionasindexedby Further, the three-way interaction for Task-by-
SCRandEMG,andfearconditioningbutnotextinction Phase-by-Anxiety group also was significant, F(2,
based on self-reported fear; however, further analyses 152) 3.49, P .033, partial η2 .044 (Fig. 3). This
= = =
wereconductedtounderstanddifferencesbetweentasks. interactionwasdecomposedaccordingtoanxietygroup,
DepressionandAnxiety
ResearchArticle:ExaminingaNovelDevelopmentallyAppropriateFear-ConditioningTask 283
Figure2.Fearconditioningandextinctioninanxiousandnonanxiousparticipantscollapsedacrossageandtasks.
yielding a significant Task-by-Phase interaction only whereas in adults this differential effect was stronger
amonganxioussubjects,F(2,72) 5.21,P .008,partial whenthebelltaskwasadministeredfirst.
η2 .127. This interaction der=ives from=higher levels
=
ofself-reportedfearofanxiousparticipantstothesocial SCR
stimuli (CS) used in the screaming lady compared to
TheANOVAonSCRyieldedasignificantfour-way
bellsevenpriortoconditioning,t(36) 3.31,P .002.
= = interaction with Task-by-Phase-by-Stimuli-by-Age,
Finally, the five-way interaction for Task-by-Phase-
F(2, 146) 3.87, P .024, partial η2 .10. This
by-Stimuli-by-Agegroup-by-Orderwassignificant,F(2, = = =
interaction was decomposed to a three-way Task-by-
152) 5.82, P .004, partial η2 .07. Decomposing
= = = Phase-by-Stimuli interaction according to age group,
this interaction by isolating phase, age group, and or-
resulting in nonsignificant results in both age groups.
derinsuccessivestepsrevealedthatthebelltaskelicited
However,theinteractionbetweenPhase Stimuliwas
stronger differential learning effects (CS > CS ) in ×
+ − significant in youth, F(2, 50) 5.59, P .006, partial
youthwhenthescreamingladytaskwasdeliveredfirst, η2 .18, but not in adults, F(=2, 96) 1=.92, P .153,
= = =
DepressionandAnxiety
284 Shechneretal.
Figure3.Theeffectoftask,phase,andanxietygrouponself-reportedfear.
partialη2 .04.Further,inyouth,SCRwashigherfor that, among adult participants, the screaming lady did
=
CS compared to CS during conditioning in both notelicitdifferentiallearningbetweentheCS andthe
+ − +
tasks (all Ps < 0.029), but there were no differences CS asindicatedbylevelsofSCR.
−
in SCR during extinction (all Ps > .297). Finally, a
conditioning effect was obtained in adults only in the FPS–EMG
belltaskt(51) 1.85,P .046,butnotinthescreaming
= = The ANOVA on EMG yielded a significant six-
ladytask,t(51) .76,P .450(Fig.4).Resultsindicate
= = wayinteractionwithTask-by-Phase-by-Stimuli-by-Age
Figure4.Theeffectoftask,phase,stimuli,andagegrouponSCR.
DepressionandAnxiety
ResearchArticle:ExaminingaNovelDevelopmentallyAppropriateFear-ConditioningTask 285
group-by-Anxiety group-by-Order, F(4, 296) 2.75, A basic premise in the fear-conditioning literature is
P .029, partial η2 .036. This interaction =was de- that individual differences in fear conditioning and ex-
= =
composed by isolating it according to its factors. This tinction are trait-like patterns of responding that show
processrevealedtheinteractiontoarisefromoneunusu- stabilityovertime.However,tothebestofour knowl-
allystrongfindinginaparticulargroup.Namely,thebell edgeonlythreepreviousstudies,allinadults,examined
task elicited stronger differential learning effects (CS thetemporalstabilityoftheseindices.[18–20]Resultsfrom
+
>CS )inanxiousyouth,relativetoothergroups,when thepresentstudyaregenerallyinlinewiththeseprevious
−
itwasdeliveredafterthescreamingladytask. studiesindicatingmoderatestabilityovertime.Interest-
ingly, research implies that temporal stability is better
whentestedintwodifferentsetsofstimuli,aswasdone
inthecurrentstudy.[18]Futurestudiesaimingtoexamine
DISCUSSION
changes in fear conditioning and extinction over time,
Thisstudyisthefirsttoexaminedifferencesbetween forexample,beforeandaftertreatment,mightconsider
anxious and nonanxious youth andadultsusinganovel usingdifferentstimuli,suchasthestimulifromthetwo
bell-based fear-conditioning task. The study also com- tasksusedinthecurrentstudy.However,asdiscussedin
pared findings on this novel task to findings on a well- thenextsection,differencesinthesocialandnonsocial
validatedscreamtask.Bothtaskswereequallywelltoler- natureofthestimulishouldbeconsidered.
atedinpediatricandclinicalpopulations,andbothtasks
elicitedfearresponseswithmoderatestability,asindexed
bycorrelationsbetweenthetwotasks. FEARCONDITIONINGANDEXTINCTIONIN
Wefirstdiscusstheresultsforanxiousandnonanxious ANXIOUSANDNONANXIOUSYOUTHAND
youth and adults collapsed across tasks. We then dis- ADULTS
cussthespecificfindingsthatemergedforthetwotype Themaineffectofanxietyonself-reportedfearfound
oftasksusedinthepresentstudy.Threemainfindings in the current study is similar to results in two previ-
emerged from this set of results. First, anxious partici- ous studies that used the screaming lady task, in which
pantsreportedgreaterfeartobothCSsthannonanxious anxious participants reported greater fear to both CSs
participants.Second,comparablefear-conditioningand thannonanxiousparticipants.[1,5]Yet,inapediatricstudy
extinction effects were obtained in all groups (healthy that used a different conditioning paradigm with ge-
and anxious, adults and children) on self-reported fear ometric shapes, anxious children rated the valence of
andFPS(EMG),butonlyinyouthonSCR.Third,some theCS morenegativelythannonanxious childrenaf-
+
differencesacrossthetwotaskswereobservedasafunc- ter conditioning and extinction, but no main effects of
tionoftaskdeliveryorder. anxiety emerged for the CS or for differential fear.[4]
−
Oneofthegoalsofthisstudywastovalidateanovel Therefore, the inconsistent results concerning extinc-
conditioning task using a bell as a UCS by comparing tioncouldhaveresultedinlowerlevelsofreportedfearto
findingsonthistaskwithapreviouslyusedscreamtask. nonsocial(e.g.,geometricshapes)thanthesocialstimuli
Specifically, compared to Britton et al.,[1] the attrition usedinthescreamingladytask,particularlyamonganx-
rates in the current study for both the screaming lady iousparticipants.Inaddition,previousstudiesinanxious
and the bell tasks were relatively low with few partici- children[4,6] andadults[2] reportamaineffectofanxiety
pantsabortingeitherfear-conditioningtask.Thislower not only on self-reported fear but also on other psy-
ratecouldbeattributedtotherelativelysmallsamplesize chophysiological indices such as SCR and FPS, effects
inbothstudiesaswellassomelevelofhabituationtore- notseeninthecurrentstudy.Insummary,generallevels
peated administration of the tasks in the current study. ofheightenedfearduringfearconditioningandextinc-
Completionratesalsowerecomparedamongyouthwho tion are observed in anxious compared to nonanxious
underwentthescreamtaskfirstinthecurrentstudy,rela- youthandadults.
tivetoratesfromthepreviousstudy.[1]Inthesecontrasts, Although perturbations in fear conditioning and ex-
nodifferencesemergedforthenonanxiousgroup,buta tinction are thought to play a role in the etiology and
significantdifferencedidemergefortheanxiousgroup. maintenanceofanxietydisorders,resultsinthecurrent
Attrition rates in anxious children were higher for the studyindicatethatbothanxiousandnonanxiousindivid-
screamtaskinthepreviousstudy,ascomparedwithattri- ualshavecomparablelevelsofdifferentialconditioning
tionratesforanxiouschildreninthecurrentstudy.Yet, andextinction,asmeasuredbyallthreedependentvari-
thesamplesizeinthecurrentstudywassmall.Moreover, ables.Theseresultsfurthersupportpriordiscriminative
whenthecurrentstudydirectlycomparedreportedanx- fear-conditioningstudiesinadults.[2]However,findings
ietyacrosstasks,themaineffectoftaskwassignificant, in the current study and other studies in pediatric anx-
with the scream eliciting more fear than the bells. Fu- iety disorders show similar effects in conditioning but
ture studies with larger samples should further address differenteffectsinextinction.Thatis,allofthepediatric
theimportantquestionofcomparingthetolerabilityof studies,likethestudiesinadults,failedtofinddifferences
thetwotasks.Nevertheless,basedondataacrossthetwo betweenanxiousandnonanxiouschildrenindifferential
studies,thebelltaskappearstobebettertoleratedthan learningduringfearconditioning.[1,4–6]Yet,thecurrent
thescreamtask. findings differ from previous reports in which anxious
DepressionandAnxiety
286 Shechneretal.
children exhibit extinction-related deficits in SCR and overall SCR response in youth than adults) have been
FPS,ascomparedtononanxiouschildren.[4,6,7]Inthese reported in previous fear-conditioning studies.[1,5] Fi-
studies, anxious children, but not healthy participants, nally,thisdifferentialconditioningacrossthetwotasks
showed larger SCR and FPS to CS than CS after couldrelatetodifferencesinphysiologicalresponsesto
+ −
extinction, indicating resistance to extinction. Finally, theneutralCSusedinthebelltask(bellcartoons)com-
based on self-reported fear both anxious and nonanx- paredtothescreamingladytask(humanface),withthe
iousparticipantswerenotextinguished.Thelackofex- latterelicitinghigherlevelsofSCRtotheCS .
−
tinction, as indexed by self-report, was also evident in Along the same lines, the order in which the tasks
ourfirsttwostudieswiththescreamtask.[1,5]Moreover, were administered in the present study had no effect
although not widely discussed, prior studies repeatedly on SCR but did affect self-reported fear and FPS. The
show that subjects’ verbal reports regarding condition- belltaskelicitedstrongerdifferentiallearningeffects,in-
ingexperiencesdonotreflecttheirautonomicresponses, dexedbyself-reportedfear,inyouthwhenthescreaming
withpatternsthatappearquitesimilartothepatternsin ladytaskwasdeliveredfirst.Conversely,inadultsdiffer-
ourpasttwostudies.[21–24] ential learning was stronger in the screaming lady task
Several methodological differences among studies whenthebelltaskwasadministeredfirst.Moreover,anx-
may explain their differing results. Studies identifying iousyouthshowedstrongerdifferentialeffectsinthebell
extinction-related effects used nonsocial stimuli (geo- taskindexedbyEMGwhenthescreamingladytaskwas
metricshapesorcartoonfigures);whereasparadigmsus- deliveredfirst.
ing social stimuli did not show these extinction-related Strong differential conditioning effect depends on a
effects using SCR. As discussed below, task-based dif- potent and ecologically valid UCS paired with neutral
ferences were also found in the current study. Taken stimuli. If indeed a screaming lady UCS is more po-
together,itappearsthatfearconditioningelicitscompa- tent than a bell UCS, stronger conditioning effects are
rabledifferentiallearningbetweenanxiousandnonanx- expected to arise, particularly in adults who completed
ious youth during fear conditioning. Nevertheless, dif- thistaskafterthebelltask.Yet,socialstimuliaremore
ferences in extinction appear to vary as a function of salienttochildrenandevenmoresotoanxiouschildren.
outcome measure, study paradigm, and sample charac- Thus, the stimuli used in the bell task could have been
teristics. perceivedasmoreneutralthanthefacesinthescreaming
lady task, resulting in a stronger differential condition-
ingeffect.Thiseffectcouldhavebeenexacerbatedbythe
TASK-SPECIFICRESPONSES orderofthetasks,asparticipantsknewwhattoexpectin
Differences in stimuli could explain other discrepant thesecondtask,whichmayhavecontributedtogeneral
findings across the two tasks obtained in the current levelsofdecreasedfear.
study. For example, the difference in self-reported fear
betweentheCS andCS wasgreaterinthebelltask
thaninthescrea+minglady−task,again,duetohigherlev- LIMITATIONS
els of fear elicited by the social CS in the screaming Although the present study compared anxious and
−
ladytaskrelativetothenonsocialCS inthebelltask. nonanxious youth and adults on two different fear-
−
Similarly,anxiousparticipantsreportedhigherlevelsof conditioning tasks using three dependent variables,
feartothesocialstimuliusedinthescreamingladytask several limitations should be noted. First, the sample
comparedtothenonsocialstimuliusedinthebelltask, sizes were relatively small, particularly for the anxious
even prior to the fear acquisition phase (precondition- youth. This may have limited our ability to observe
ing). between-group differences in fear conditioning and
Differential SCR responses to the CS versus CS extinction.Smallsamplesizealsoprohibitedourability
+ −
infearconditioningamongadultswereobservedinthe to test for potential differences between anxiety sub-
belltask,butunexpectedly,werelackinginthescream- types, which may be relevant given differences in fear
ingladytask.Thiseffectissurprisinggiventhatprevious conditioning between anxiety subtypes in adults.[25,26]
studies using this,[1,5] and similar tasks consistently re- However, despite modest sample sizes, the study
portdifferentialconditioninginSCR.[2]Onepossibility acquired a considerable amount of data from over 150
thatmayaccount,atleastpartially,forthelackofSCR- conditioningandextinctionsessions.Asecondlimitation
conditioningeffectsinadultsinvolvestheinclusioncri- relevant to sample selection is that all participants who
teriaappliedinthecurrentstudy.Somepreviousstudies completed the fear-conditioning and extinction phases
excludeSCRnonresponders;[2]however,allindividuals, successfully were included in the analysis, irrespective
includingrespondersandnonresponders,wereincluded of whether they learned the CS-UCS contingency or
here,sincethesesubjectsprovidedusefuldataforEMG showed differential conditioning as indexed by SCR or
and self-reported fear. Indeed, the rate of SCR nonre- FPS. Although this approach allows findings to better
sponders was higher in adults (26.2%) than in youth representthegeneralanxietypopulation,itcouldreduce
(5.3%). Another possibility is age differences in SCR. ourabilitytodetectsomebetween-groupdifferences.
Overall, levels of adult SCR were lower than in chil- Other limitations relate to methodological con-
dren. Such age-related differences in SCR (i.e., greater straints of data acquisition. First, we did not obtain
DepressionandAnxiety