Baseline and affective startle modulation by angry and neutral faces in 4-8-year-old anxious and non

35 Pages·2017·0.28 MB·English

Baseline and affective startle modulation by angry and
neutral faces in 4-8-year-old anxious and non-anxious
children
Author
Waters, Allison M, Neumann, David L, Henry, Julie, Craske, Michelle G, Ornitz, Edward M
Published
2008
Journal Title
Biological Psychology
DOI
https://doi.org/10.1016/j.biopsycho.2007.12.005
Copyright Statement
© 2008 Elsevier. This is the author-manuscript version of this paper. Reproduced in accordance
with the copyright policy of the publisher. Please refer to the journal's website for access to the
definitive, published version.
Downloaded from
http://hdl.handle.net/10072/21264
Link to published version
http://www.sciencedirect.com/science/journal/03010511
Griffith Research Online
https://research-repository.griffith.edu.au
Startlemodulationinchildhoodanxietydisorders 1
Baseline andAffectiveStartleModulationbyAngryandNeutral Faces
in4-8Year OldAnxiousandNon-Anxious Children
Allison M. Waters1,David L.Neumann1,JulieHenry1,
MichelleG.Craske2, & EdwardM. Ornitz3
1School ofPsychology, GriffithUniversity,Gold Coast,Australia
2Department ofPsychology,UniversityofCalifornia, Los Angeles, USA
3Department ofPsychiatryand Biobehavioral Sciences, UniversityofCalifornia,
Los Angeles, USA
Address forCorrespondence:
Allison M. Waters Ph.D.,School ofPsychology, GriffithUniversity,Gold Coast Qld4222,
Australia.Phone: [phone],Email: [email protected]
Startlemodulationinchildhoodanxietydisorders 2
Abstract
Thepresent studyexaminedthemagnitudes ofstartleblinkreflexes andelectrodermal responses
in4to8 yearold high anxious children (N=14)andnon-anxious controls (N=11).Responses
were elicitedby16auditorystartletrials duringa baselinephasepriortoan affectivemodulation
phaseinvolving12startletrials presentedduringangryandneutral faces. Results showed
significant responsehabituationacross baselinetrials and equivalent responsemagnitudes
between groups duringthebaselinephase.Themodulationofresponsemagnitudes duringangry
andneutral faces didnot differsignificantlyineither group.However, highanxious children
showedlargerresponses overall comparedwith non-anxious control childrenduringthe
affectivemodulation phase. Moreover, greater anxietyseverityandlarger startlereflexes were
associatedwithpooreraccuracyin ratingneutral faces as neutral inhighanxious children.
Results mayreflect elevatedreactivitytothreat contexts in 4to 8 yearold high anxious versus
non-anxious children.
Startlemodulationinchildhoodanxietydisorders 3
Baseline andAffectiveStartleModulationbyAngryandNeutral Faces
in4-8Year Old AnxiousandNon-Anxious Children
Anxietydisorders arethe most commonlydiagnosed psychiatricdisorders andoneofthe
most significant healthproblems interms ofglobal burdenofdisease,exceedingthevast
majorityofphysical healthdiseases (Murray& Lopez,1996). Childhood-onset anxietyis a
debilitatingconditionaffectingupto15-20%of youths and is asignificant risk factorforother
emotional andbehavioural disorders includingadolescent andadult anxiety(McGee,Feehan,
Williams, &Anderson, 1992),depression(Hayward,Killen,Kraemer, &Taylor,2000; Pine,
Cohen,Gurley, Brook, & Ma1998),eatingdisorders (Patton,1998)andsubstancedisorders
(Merikangas, Avenevoli, Dierker, &Grillon, 1999).Childhoodanxietydisorders arealso
associatedwithdebilitatingacademicandvocational functioning(Kessler, Foster,Saunders, &
Stang,1995),impairedsocial competence(Spence,Donovan, & Brechmann-Touissant,1999),
andifleft topersist intoadulthood,arangeofsocio-economiccosts includingunemployment,
days lost from work,hospitalisationandmedication(Waghorn,Chant,White,&Whiteford,
2004).
Althoughresearchonchildhoodanxietydisorders lags behind researchon adult anxiety
ingeneral, a combination ofbothgeneticand environmental influences are thought toplay
contributoryroles tothe development andmaintenanceof childhoodanxietydisorders (see
Craske& Waters, 2005,forareview).Theunderstandingof neurophysiological processes that
underliechildhoodanxietydisorders is particularlylimitedandbasedprimarilyon studies of
childrenin mid-to late-childhoodandadolescence(see Ornitz,1999,forreview).Thecurrent
studyextends this literaturebyexaminingbaselineandaffectivemodulation ofthestartlereflex
inhigh anxious andlowanxious control childrenbetween4 and8 years of age.
Startlemodulationinchildhoodanxietydisorders 4
Themagnitudeofthehumanstartlereflex indexes defensiverespondingtoaversive
stimuli andassociated contexts (seeDavis, 1998,and Grillon& Baas, 2003,forreviews).
Rodent studies haveshownthat modulationofthestartlereflex byaversivecontexts (suchas
longdurationbright lights)is mediatedbythebed nucleus ofthestriaterminalis, whereas fear-
inducedmodulationofthestartlereflex byexplicit threat cues (such as acuepreviouslypaired
withan electricshock)is mediatedbythecentral nucleus oftheamygdala (Davis, 1998; Walker,
Toufexis, &Davis,2003). As tendencies to react withfear andavoidanceinarangeofsituations
associatedwithanxiety-provokingstimuli arehallmarks ofemotional andbehavioural
characteristics of anxiouschildren (AmericanPsychiatricAssociation,1994), thestudyofstartle
reflex modulationbyexplicitlyaversivestimuli and associatedcontexts mayelucidatethe
neurophysiological processes that underlieanxietydisorders inchildren.Moreover, as an
involuntaryresponsepresent from birth,thestartlereflex is aneurophysiological measure
especiallysuitedto thestudyofdefensiverespondingin youngchildren (seeOrnitz,1999,fora
review).
Numerous studies havedemonstratedincreasedstartlereflex magnitudein adults with
anxietydisorders incontexts associatedwiththreat but not inresponseto explicit threat cues.
Forexample,Grillonand colleagues demonstrated that adults withpanicdisorderandpost-
traumatic stress disorder (PTSD) showed sustained elevations in “baseline” startlereflexes
elicitedat thecommencement oftheexperimental sessionthat laterinvolvedthedeliveryof
unpleasant electricshocks signalledbya cue. In contrast,participants with anxietydisorders did
not differfrom controls in startlereflex magnitudewhenelicitedduringexplicit cues ofthreat
(e.g., Grillon,Ameli,Goddard,Woods, &Davis, 1994; Grillon,Morgan, Davis &Southwick,
1998; Grillon&Ameli 1998; Grillon&Morgan, 1999). Baselinestartlereflexes werenot
elevated whenparticipants withPTSDwereexplicitlyinformed that noaversivestimuli would
bepresentedduringtheentireexperimental procedure(e.g., Grillon et al., 1998).Anotherstudy
ofpoliceofficers (Pole, Neylan, Best,Orr, &Marmar, 2003)demonstratedthat severityof
Startlemodulationinchildhoodanxietydisorders 5
PTSDsymptoms correlatedwith startlereflex magnitudeduringlowandmedium threat
conditions, wheninformedthat noshockwouldbedelivered,but didnot correlate with startle
reflex magnitudeduringhighthreat conditions that explicitlysignalledpotential shock.Thus, in
all ofthesestudies, adults with anxietydisorders did not showlargerstartlereflexes compared
withlowanxious adults inresponsetocues signallingexplicit threat ofelectricshock. Instead,
theyshowedelevatedrespondingincontexts associatedwiththreat (seeGrillon,2002).
Elevatedbaselinestartle reflexes inindividuals with anxietydisorders is thought to
represent increasedanxietyabout thelaboratorycontext associatedwiththreat of anaversive
stimulus (Grillonet al., 1998b). Indeed, Grillon,Baas, Lissek,Smith,and Milstein (2004)
concluded that “sustained contextual anxiety, but not phasic explicit cue fear, differentiates
anxiety-disorderedfrom non-anxiety-disordered individuals” (p.916).This conclusionreflects
what has been called the “strong situation” effect (Lissek, Pine, &Grillon, 2006),inwhich
anxious andnon-anxiousindividuals respond equallytointenselyaversive stimuli,whereas only
anxious individuals also respond stronglyto lowintensityaversivestimuli relativetonon-
anxious individuals.
Asmall literatureexists onfear-potentiated startlemodulationin children with most
studies basedonchildren at risk foranxietydisorders byvirtueofparental anxiety. For example,
childandadolescent offspringofparents withanxietydisorders (agerange 7to18 years)have
exhibitedelevatedstartle reflexes duringtheprecedingbaselinephase as well as during
darkness-inducedfear-potentiationprotocols andduringthreat ofan airblast tothelarynx
comparedwith low-risk offspring(Grillon,Dierker,&Merikangas, 1997; 1998; Merikangas et
al.,1999). Similarly,whereas therewereno group differences in startle reflex magnitudes
duringpictures offear-relevant visual (i.e.,snake picture)and auditory(i.e.,1000Hz,100dB
tone)stimuli,offspringofanxious parents (age range7to12 years)displayedsignificantly
higher electrodermal activityduringtherestingbaselineandduringtheinter-trial intervals
(Turner, Beidel,&Roberson-Nay,2005).
Startlemodulationinchildhoodanxietydisorders 6
Asignificant limitationin applyingfear-potentiationprotocols with youngchildrenis
that threat ofelectricshock,airblasts tothelarynx, and periods oftimeincompletedarkness
maybetooaversivefor youngchildrentotolerate. Oneavenueforovercomingthis limitation
has beento employapictureviewingparadigm that assesses affectivemodulationofthestartle
reflex (e.g., Bradley,Cuthbert,& Lang,1993; Cuthbert,Bradley, & Lang, 1996).Anextensive
literaturewithadults has shownrepeatedlythat blinkreflexes arelargerwhileviewing
unpleasant pictures incomparison toblinks elicitedduringneutral andpleasant pictures
(Cuthbert et al.,1996).Affectivemodulationoftheblinkreflex is thought toreflect the
activationofdefensivemotivational processes bythematchinaffectivevalencebetween
unpleasant picturestimuli andtheaversiveauditorystartle-elicitingstimulus (Bradley,Cuthbert,
& Lang,1999). Moreover,adult studies havedemonstratedarobust relationshipbetween
enhancedaffectivestartle modulationandhighfearfulness (e.g.,Cook,Hawk,Davis, &
Stevenson, 1991; Hawk, Stevenson, &Cook,1992).
Studies ofaffectivemodulationin normallydevelopingchildrenhaveproduced results
divergent from thosewithadults. McManis andcolleagues wereunabletodemonstratestartle
facilitationduringunpleasant compared withneutral pictures in7to10 year oldchildren (e.g.,
McManis, Bradley,Cuthbert,and Lang,1995)andfoundthat girls but not boys showedthe
expectedincreaseinstartlereflex magnitudeduringunpleasant thanpleasant pictures
(McManis, Bradley, Berg,Cuthbert,and Lang(2001).Cook,Hawk,Hawk,andHummer(1995)
also didnot findtheadult patternusingaffectivelyvalent script-induced imageryinschool-age
children; almost identical startlemagnitudewas foundduringimageryofpleasure,joy,sadness,
fear, andanger.Finally, Waters, Lipp,andSpence(2005)foundthat startlereflex magnitudedid
not differsignificantlyduringunpleasant comparedwith neutral orpleasant pictures in8to12
yearoldchildren.
Studies examininganxiety-related differences in affectivemodulation ofstartlein
children have also producedconflictingresults.Cooket al.(1995)foundthat startleresponses of
Startlemodulationinchildhoodanxietydisorders 7
childrenwhoscoredhigheronafearsurveyscheduleweresmallerduringunpleasant than
pleasant imageryandweresmallerinhighfearcomparedwith lowfearchildren.Waters et al.
(2005)foundthat anxious childrenshowedlarger blinkreflexes overall duringunpleasant,
neutral andpleasant pictures comparedwithlow anxious children.As affectivestartle
modulationis strongest forstartlereflexes elicitedduringhighlyarousingaffectivestimuli
(Cuthbert et al., 1996),inconsistent results betweenchildrenandadults havebeen attributedto
theless arousingpicture stimuli usedwithchildrencomparedwithadults andtheunreliabilityof
imageryprocedures withchildren (seeMcManis et al.,2001; Waters et al., 2005).
Emotional facestimuli inapictureviewingparadigm maybe anapproachthat
overcomes theselimitations with very youngchildren. Other advantages includethe greater
ecological validityoffacestimuli thanotheremotion-evokingstimuli (Mogg & Bradley,1998)
andthat emotional faces, suchas angryones, receivepreferential processingoverothersalient
stimuli duetotheirevolutionaryassociationwiththreat to thesafetyofhumans across the
lifespan (seeÖhman & Mineka,2001,for areview). Recent functional neuroimagingand
cognitivesciencestudies withchildrenandadolescents between8and18 years of ageshow
perturbed amygdalaactivationand attentionallocationtoangryand fearful faces compared with
neutral ones inanxious versus non-anxious youths (e.g., Hadwinet al.,2003; Stirling,Eley, &
Clark,2006; Monk et al.,2006; Thomas et al.,2001; Waters & Lipp,in press; Waters, Mogg,
Bradley,&Pine,inpress). Moreover, recent studies ofstartlemodulationbyemotional faces
withnon-selected adults demonstratedlargerstartlereflex magnitudes whenparticipants viewed
angryfaces versus othertypes ofexpressions (i.e., fearful,neutral, andhappy) (Springer,Rosa,
McGetrick, & Bowers, 2007).Thesefindings suggest that emotional faces maypossess greater
sensitivitythanbroad-basedaffectivepicturestimuli forassessingneurophysiological processes
that underlieanxietyinchildren,suchas enhanceddefensiverespondingtothreat andassociated
contexts.
Thepresent study
Startlemodulationinchildhoodanxietydisorders 8
This studyexamined baselineand affectivestartle modulation in young anxious andnon-
anxious childrenbetween 4 and8 years ofage.This agerangewas selected toexpandon
previous studies that havenot assessedchildren below7-8 years ofage. Thestudyassessed
whetherhighanxious children wouldshowlarger startlereflexes compared with non-anxious
control childrenduringa baselinephasepriorto an affectivemodulation phaseinwhichangry
faces werepresented.Thestudyalso examinedwhetherhighanxious children wouldshow
enhanced affectivestartle modulation relativeto non-anxious control children,as indexedby
largerstartlereflexes duringangrycomparedwith neutral faces.Angryfaces wereselected
becausetheyarestronger signals ofthepresenceofthreat than are fearful faces (Whalen et al.,
2001)andhavebeenshowntoelicit largerstartlereflex magnitudes than fearful,happyor
neutral expressions inadults (Springer et al.,2007).Moreover,in theabsenceofaffective
modulationstudies inchildrenusingfacestimuli,wecomparedresponses duringangryfaces
withthoseduringneutral faces basedonthe cognitivescienceliteraturewhichhas shown
reliableanxiety-relatedattentional bias effects for angryfaces compared withneutral ones in
children(e.g., Hadwinet al.,2003; Stirlinget al.,2006; Monk et al.,2006; Waters et al.,in
press).Skinconductance responses were also recordedas an adjunct orcomplementarymeasure
tothestartleblink reflex becauseit will reflect adefensiveresponsetothestartleeliciting
stimulus. Similarresults across thetwomeasures were expected.
Method
Participants
Participants were25 childrenaged 4 years, 4months to8 years, 6months (12 girls; 13
boys).Ofthese children, 14hadaclinically-significant diagnosis ofananxietydisorder(Mage
=6.08,SD=1.44; 7 girls; 7boys)and11 werenon-anxious controls (Mage=6.00; SD=1.41;
5girls; 6boys).Writteninformedconsent was obtained from parents priorto children’s
participationinanexperimental protocol that was approvedbythe Institutional Human
Research Ethics Committee. Highanxious childrenwere referredbypaediatricians, local
Startlemodulationinchildhoodanxietydisorders 9
communitymental health agencies, school guidancecounsellors andparents to theGriffith
UniversityChildandAdolescent AnxietyDisorders ResearchProgram for assessment and
treatment.Non-anxious control childrenwererecruitedfrom first yearundergraduate
psychologystudents who hadchildren4to8 years old.Thesestudents receivedcourse credit in
exchange for their child’s participation.
All children werebornin AustraliaandspokeEnglish as theirfirst language. Twenty-
onechildren (85%)lived with parents whoweremarried and four children(16%)hadparents
whowereseparated/divorced.Childrentendedtocomefrom averageincomeAustralianfamilies
accordingto theDaniel PrestigeScale(1983), ameasureofAustralianoccupational prestige.
Therewereno significant differences between groups ondemographicvariables.
Diagnosticstatus ofhigh anxious childrenwas determinedusingtheparent interview
scheduleofthe AnxietyDisorders InterviewScheduleforDSM-IV (ADIS-C; Silverman &
Albano,1996)inwhicha clinicianseverityrating(CSR)of4orgreater(scale0to8)for at least
theirprincipal diagnosis was usedtodetermineclinical significance (Silverman&Albano,
1996).Thus, inclusion criteriaforanxious children was aprincipal diagnosis ofananxiety
disorderwithanADIS-C CSR of4orgreater,intheabsenceof externalisingdisorders,
developmental disorders, psychosis, organicbraindamageorvisionimpairments. Major
depressivedisorder(MDD)was not a reason forexclusionas longas it was not theprincipal
diagnosis.Nochildmet criteriaforMDD.Thus, of the14high anxious children,six had a
principal diagnosis ofspecificphobia, threehad generalised anxietydisorder, threehad
separationanxietydisorder,andtwohadsocial phobia.ThemeanADIS-C CSR of children’s
principal anxietydiagnosis was 6.43(SD=1.91)and comorbiditybetween anxietydisorders
was high with childrenhavinganaverageof3.64 anxietydiagnoses (SD = 2.13),predominantly
specificphobias.Thesixchildrenwithaprincipal diagnosis ofspecificphobiaall hadcomorbid
diagnoses ofeither generalisedanxietydisorder,social phobiaorseparationanxietydisorder,
suggestingthat emotional faces wouldbeas pertinent tothesechildren as thosewithprincipal