Social Adversity and Antisocial Behavior

12 Pages·2017·0.37 MB·English

by  Shawn E. Fagan

JAbnormChildPsychol
DOI10.1007/s10802-017-0262-0
Social Adversity and Antisocial Behavior: Mediating Effects
of Autonomic Nervous System Activity
ShawnE.Fagan1,2&WeiZhang3&YuGao1,2
#SpringerScience+BusinessMediaNewYork2017
Abstract Thedisplayofantisocialbehaviorsinchildrenand Keywords Heartrate .Gender.Antisocialbehavior.Social
adolescents has been of interest tocriminologists and devel- adversity.Arousal .Aggression
opmentalpsychologistsforyears.Exposuretosocialadversity
is a well-documented predictor of antisocial behavior.
Antisocial behaviors and callous-unemotional/psychopathic
Additionally, measures of autonomic nervous system (ANS)
traits constitute a predominant risk factor for future criminal
activity, including heart rate variability (HRV), pre-ejection
behavior (Dyck etal. 2012). Earlylife displays of antisocial
period(PEP),andheartrate,havebeenassociatedwithanti-
behavioroftenpersistintoadolescenceandadulthood(Moffitt
social behaviors including rule-breaking and aggression.
and Caspi 2001), which makes early intervention critical as
Social neuroscience research has begun to investigate how
well as difficult. Propagation of such behavior is often rein-
neurobiologicalunderpinningsaffecttherelationshipbetween
forcedinhighcrimeareas,representingacounter-cultureat-
socialadversityandantisocial/psychopathicbehaviorinchil-
titudethatsupportsaggressivebehaviorandmistrustofsoci-
dren and adolescents. This study investigated the potential
etalrules(Ingoldsbyetal. 2006;Simonsetal. 2012).Social
mediatingeffectsofANSactivityontherelationshipbetween
neuroscience perspectives on antisocial behavior and risk-
socialadversityandantisocialbehaviorinagroupof7-to10-
taking have begun to investigate how neurobiological pro-
year-oldchildrenfromthecommunity(N=339;48.2%male).
cessesinfluence the relationshipbetweenearly-lifeexposure
Moderatedmultiplemediationanalysesrevealedthatlowrest-
tosocialadversityandpersistentbehavioraldeficitsthatmay
ingheartrate,butnotPEPorHRV,mediatedtherelationship
resultinfuturecriminaloffending(Choyetal.2015).
betweensocialadversityandantisocialbehaviorinmaleson-
ly. Social adversity but not ANS measures were associated
with antisocial behavior in females. Findings have implica-
tionsforunderstandingtheneuralinfluencesthatunderliean- SocialAdversityandAntisocialBehavior
tisocialbehavior,illustratetheimportanceofthesocialenvi-
ronment regarding the expression of these behaviors, and Socialadversity,anumbrellatermthatreferstoissuessuchas
highlightessentialgenderdifferences. violentcrime,segregation,exposuretodelinquentpeers,pover-
ty, and poor parenting (Beaver et al. 2008; Moffitt and Caspi
2001;ScarpaandOllendick2003),isoneofthestrongestrisk
* ShawnE.Fagan factorsfordevelopingantisocialbehavior.Earlyandcontinued
[email protected] exposuretosocialadversityhasdetrimentaleffectsfordevelop-
ingyouth,andcanexacerbatepreexistingbehavioralissues(Liu
1 DepartmentofPsychology,TheGraduateCenter,CityUniversityof 2004).Researchshowsthattheprogressionofantisocialbehav-
NewYork,3655thAve,NewYork,NY10016,USA iorandsubsequentdelinquencyisshapedbyantisocialattitudes
2 DepartmentofPsychology,BrooklynCollege,CityUniversityof (Millsetal.2004),poorschoolingandalackofcollectiveeffi-
NewYork,2900BedfordAvenue,Brooklyn,NY11210,USA cacyinthecommunity(Ingoldsbyetal.2006),delinquentpeer
3 QueensCollege,CityUniversityofNewYork,65-30KissenaBlvd, affiliationsduringadolescence(Monahanetal.2009),andmal-
Flushing,NY11367,USA nutrition (Raine et al. 2003). Behavioral genetic studies have
JAbnormChildPsychol
also demonstrated that shared and non-shared environmental and externalizing behaviors in situations of familial adversity
influences play significant roles in predisposing individuals to (Beauchaineetal.2007).LowrestingHRVhasbeenassociated
antisocialbehavior(i.e.,Eleyetal.2003).Inaddition,thesocial with outcomes in children such as antisocial behavior
environment influences biological risk factors that have been (Mezzacappaetal.1997),externalizing(Pineetal.1998),reac-
linkedtoantisocialandcriminalbehavior. tive aggression (Scarpa et al. 2010), and oppositional defiant
disorder and conduct disorder (Beauchaine et al. 2007). On
the other hand, some studies have shown that high resting
LowHeartRateandAntisocialBehavior HRVisassociatedwithincreasedproactiveaggression(Scarpa
etal.2010)andexternalizingbehavior(Dietrichetal.2007).
Lowrestingheartrate(HR)isoneofthemostrobustandwell- Pre-ejectionperiod(PEP)isawidelyusedmeasureofsym-
replicatedbiologicalmarkersofantisocialbehavior(Ortizand patheticrelatedcardiacactivitythatmeasuresthetimefromthe
Raine2004),andhasbeenlinkedtoproactiveandinstrumen- depolarization of the left ventricle of the heart to the onset of
tal aggression (Ortiz and Raine 2004; Scarpa et al. 2010), ejection of blood into the aorta, and represents cardiac output
callous-unemotionaltraits(FrickandWhite2008),antisocial modulated by the beta-adrenal system (Berntson et al. 1994;
behavior (Mezzacappa et al. 1997), and rule-breaking/delin- Musser et al. 2013). Lengthened resting PEPs (reflecting low
quency(Jenningsetal.2013).Theoriesofunder-arousaland sympathetic activity) have been correlated with conduct prob-
sensation-seeking speculate that individuals with hypoactive lemsandaggression(Beauchaineetal.2013),externalizingbe-
autonomicnervoussystem(ANS)activity(i.e.,thosewithlow havior(BrennerandBeauchaine2011),andoppositionaldefiant
resting HR) participate in risky or thrill-seeking behaviors disorder and attention deficit hyperactivity disorder (Crowell
and/or proactive displays of aggression in an attempt to ele- etal.2006),suggestingsympatheticunder-activityinchildand
vate their autonomic arousal to more comfortable levels adolescentpopulationswithexternalizingbehavioralprofiles.
(Scarpa and Raine 2004). Alternatively, fearlessness theory
proposesthatlowlevelsofarousalreflectafearlesstempera-
ment;alackofinternalarousalthatwouldotherwisecuebodi- SocialAdversityandAutonomicFunctioning
ly structures involved in feedback and associative learning
impairsfearprocessing(Hawesetal.2009). Socialadversitymayplayaroleinalteringordisruptingbiolog-
icalfunctioning.Earlysocialadversitymayactdirectlyonthe
developinghypothalamic–pituitary–adrenal(HPA)axistoblunt
ParasympatheticandSympatheticNervousSystem stressresponses(e.g.,lowcortisolandreducedHRreactivity),
ActivityandAntisocialBehavior whichinturncanleadtoantisocialbehavior,risk-taking,impul-
sivityandpooremotionregulation(Lovallo2013).Forexam-
There is a research gap concerning the potentially separable ple,exposuretocommunityviolencehasbeenassociatedwith
effects of the sympathetic and parasympathetic nervous sys- lowrestingHRinurbanschool-agedchildren(Krenichynetal.
temsonantisocialbehavior.Therhythmoftheheartismod- 2001).Inaddition,adolescentfemalesexposedtochildmaltreat-
ulated by both sympathetic and parasympathetic inputs that mentshowedlowerrestingvagaltonethancontrols(Miskovic
accelerateandslowtheheartbeat,respectively.Thebalanceof etal.2009),andarecentmeta-analysisfoundthatchildrenfrom
thesetwosystemsiscriticalforthe developmentand execu- clinicalorat-risksampleshadreducedvagaltonecomparedto
tion of socially adaptive functions such as approach, avoid- communityandnon-clinicalsamples(GrazianoandDerefinko
ance,andarousal(ThayerandSternberg2006).Thepolyvagal 2013). However, no relationship between social adversity and
theory (Porges 1995, 2007) argues that the parasympathetic sympatheticcardiacactivityhasbeenreported.
vagalactivitythatisresponsibleforslowingtheheartactsasa Previousresearchhasfocusedmainlyonthemoderatingef-
brake,regulatingappropriateemotionalresponsestodiffering fects of cardiovascular measures on behavioral deficits from
externalandinternaldemands.Modulationsinvagalactivity stress exposure or familial adversity (e.g., Scarpa et al. 2008).
can becapturedbysignalpower inthe highfrequency band Inthesestudies,ANSactivityiscategorizedintohighandlow
derived from Fourier transformation of the HR time series groups, i.e., high versus low parasympathetic activity (El-
(Berntson et al. 1997; Porges 2007). At rest, sympathetic Sheikh and Hinnant 2011). However, few studies have exam-
and parasympathetic tone may underlie individual readiness inedhowcontinuousexposuretoearlychildhoodadversityaf-
toeitherrespond to threatorrestore bodilyhomeostasis,de- fects cardiovascular responding, which in turn leads to subse-
pendingonthesituation(Scarpaetal.2010). quent antisocial behavior. Recent evidence suggests that acute
Enhancedvagalactivityandhighlevelsofrestingheartrate and chronic stress can alter brain and bodily functioning over
variability(HRV)havebeenassociatedwithdispositionalsym- time (Lovalloetal.2012). Theneurosensitivityhypothesis ar-
pathy and concerned attention (Fabes et al. 1993). Elevated guesthatgenesandearlyenvironmentalstressexposureinteract
vagal tone can also buffer the development of internalizing withbotheachotherandthecentralnervoussystemtoinfluence
JAbnormChildPsychol
subsequent physiological activity and behavioral responsivity restingHR,itwaspredictedthattheconnectionbetweensocial
(Pluess2015).Itisnowwidelyacceptedthatdevelopmentdoes adversity and antisocial behaviors could be partially explained
notprogressaccordingtoastrictgenebyenvironmentinterac- byreducedrestingHR.Toourknowledge,onlyonestudyhas
tive process; rather, it is a function of cortical reorganization investigatedthemediatingeffectsofHRonsocialadversityand
dependentupontheenvironment,genes,andthehistoryofthe facets of criminality (Choy et al. 2015). The authors assessed
organism(CicchettiandCurtis2015).Basedonthisunderstand- various aspects of antisocial behavior in a community sample
ing of development, we would expect that neurophysiological ofchildren11–12yearsoldwhoparticipatedinastresstaskin
abnormalities such as atypical ANS activity mediate the rela- whichtheywereaskedtogivea4-minspeechfollowinga2-min
tionshipbetweenadversityandbehaviorproblems. Bpreparationphase.^ ReducedHRduringstressbutnotresting
HRwasfoundtomediatetherelationshipbetweensocialadver-
sityandantisocialbehavior(Choyetal.2015).
GenderDifferences We used a factor analytic approach to produce a single
common factor for general antisocial behavior. We focused
Currentendeavorshavesoughttofillagapintheinvestigation on a common factor measure because antisocial behavior is
and reporting of gender differences in biological research defined by both cognitive-behavioral elements and
(Clayton and Collins 2014). A meta-analysis suggests that criminogenicelements,andisreflectiveofbothcharacteristic
HR predicts antisocial behavior for both boys and girls personality traits and conduct violations/overt behaviors
(Ortiz and Raine 2004). However, of the eight studies cited (Caspi et al. 2002; Huizinga et al. 2006; Mackey et al.
thatincludedfemale-onlysamples,threefailedtodemonstrate 2016). We additionally examined mediation effects for con-
statisticallysignificantresultsforlowrestingHRasapredic- stituent subscale measures (e.g., externalizing and callous-
tor of antisocial behavior (Maliphant et al. 2003; Rogeness unemotionalbehavior)toexploreifeachhadadifferentetiol-
etal.1990).Twelvestudiesinthereviewusedmixedgender ogywithrespecttosocialadversityandANSresponding.
samples:fourdidnotshowastatisticallysignificantrelation- Second, we hoped to clarify if either parasympathetic-
ship between antisocial behavior and low resting HR (HRV)orsympathetic-related(PEP)cardiacactivitycontrib-
(DelamaterandLahey1983;Garraldaetal.1989,1991;Van utesmoresubstantiallytotherelationshipbetweensocialad-
Hulleetal.2000),threewerenotpublishedinpeer-reviewed versity and antisocial behavior. Given that low resting HRV
journals (Little 1978; Schmeck and Poustka 1995; Van has been associated with both antisocial behavior and social
Voorhees and Scarpa 2002), one did not control for gender adversity,andhighHRVhasbeenmoreconsistentlyassociat-
(Cauffmanetal.2005),andonelackedatruecontrolgroup, ed with adaptive behaviors such as emotion regulation, we
comparing only adolescence-limited antisocial behavior to predicted that low HRV would mediate the relationship be-
life-course persistent antisocial behavior, with low numbers tweensocialadversityandantisocialbehavior.Sincenorela-
of females in the life-course persistent category preventing tionship between social adversity and resting PEP has been
appropriategendercomparisons(MoffittandCaspi2001). reported,wedidnotformulateanyhypothesisonthepotential
Recentevidencesuggeststhatgendermoderatestherelation- mediatingroleofPEP.Finally,weaimedtoexploreifgender
ship between autonomic responding and antisocial behavioral moderatedthemediatingeffectsofANSfunctioningbetween
displays(Beauchaine2009),thoughthislineofinquiryisrela- socialadversityandantisocialbehavior.
tivelyunderdeveloped.OnestudyshowedthatHRatage11in
girlsdidnotcorrelatewitheffortfulcontrol,impulsivity,orag-
gressionatage16,thoughitdidforboys(Sijtsemaetal.2010). Method
Another investigation revealed that resting HR in adolescent
girlsaged16–18yearswaspositivelycorrelatedwithantisocial Participants
behaviorswhileinmalesofthesameagewasnegativelycorre-
latedwithantisocialbehaviors(Crozieretal.2008).Similarly, The sample consisted of 7- to 10-year-old boys and girls
increased electrodermal responding (a sympathetic measure) (Mean age = 9.06, SD = 0.60; 48.2% male) living in
wasrelatedtoincreasedconductproblemsinfemalesaged8– Brooklyn,NewYork,whowererecruitedaspartofanongo-
12whilelowerbaselineparasympatheticcardiovascularactivity inglongitudinalinvestigationonthedevelopmentofbehavior
wasseeninboyshighinaggression(Beauchaineetal.2008). problemsinchildhood.Flierssolicitingenrollmentinastudy
on the Bfactors that contribute to healthy and happy
childhoods^wereplacedinpublicareasandtargetedmailings
TheCurrentStudy werealsosenttoparentsofchildrenlivinginthegeographic
catchmentarea.Aphonescreeningprocesswasconductedto
The current study has three aims. First, given that both social exclude anyone that was taking medications, seeing a thera-
adversityandantisocialbehaviorshavebeenassociatedwithlow pist, had a diagnosed psychiatric disorder, intellectual
JAbnormChildPsychol
disability,orapervasivedevelopmentaldisorder.Norecords current sample was 0.87 and 0.71 for aggression and rule-
were kept for excluded individuals. A total of 445 children breaking, respectively. Externalizing Behavior is the sum of
werescreenedand 340 participated, including 52% African- therule-breakingandaggressionsubscalescores.
American, 11% Hispanic, 21% Caucasian, 2% Asian, and
14% of mixed/other. Compared to the Kings County The Antisocial Process Screening Device (APSD; Frick
(Brooklyn) or New York population, our sample consisted and Hare 2001) Caregivers completed the narcissism (7
of slightly more African-Americans, and had lower median items) and impulsivity subscales (5 items) of the APSD, a
family income ($43,200 compared to $45,215). Mean years ratingscalecomposedof20itemsthatassessespsychopathic
ofeducationofthemother(M=14.37,SD=4.11)wasslightly traitsinyouth.Caregiversareasked howwellspecificstate-
higherthanthatofthefather(M=13.19,SD=4.15,t=5.65, mentsdescribetheirchild;e.g.BEngagesinillegalactivities,^
p < 0.001). Fifty-nine percent of children lived with both andBBecomesangrywhencorrectedorpunished.^Itemsare
biologicalparents,and29%livedalonewiththeirbiological ratedona3-pointscale(0=notatalltrue,1=sometimestrue,
mother.Ofthefamiliesinwhichbiologicalparentswerenot 2=definitelytrue).Subscalescoreswerederivedbysumming
livingtogether,9%hadremarriedatthetimeofthestudy.Two therawscoresfromeachitem.TheAPSDhasdemonstrated
percentofchildrenlivedinasingle-parenthousehold,andthe validity asa representativemeasure ofpsychopathictraitsin
remaining 1% resided with a single parent and other adults youth in both community and arrested samples (Falkenbach
(often grandparents). One child was excluded from the final etal.2003;Fricketal.2000).TheAPSDcallous-unemotional
sampleduetomissingphysiologicaldata. subscale was supplemented by the Inventory of Callous-
Unemotional Traits (see below) as a measure of callous-
Procedures unemotional traits.Cronbach’s α was0.70and 0.60for nar-
cissismandimpulsivity,respectively.
We invited participants and their primary caregivers to the
university for a 2-hour laboratory assessment that included Inventory of Callous-Unemotional Traits (ICU; Frick
caregiverandchildbehavioralinterviews,neurocognitivetest- 2004;GaoandZhang2016)CaregiverscompletedtheICU
ing,psychophysiologicalrecording,andsocialriskfactoras- to assess the amount of callous-unemotional traits in youth.
sessment. Caregivers consisted predominately of biological Factor analyses on the current sample supported a modified
mothers (86.4%). All interview data were collected by ICU form with three subscales (callousness, uncaring, and
graduate-level research assistants who were trained by the unemotional) (Gao and Zhang 2016). The modified ICU
Principle Investigator. During physiological recording, chil- Scores of individual subscales and total ICU score (sum of
drencompletedanemotionlearningtask,arewardparadigm, thethreesubscalescores)derivedfromthemodifiedICUwere
andanemotionregulationtaskonthecomputer.Therewere used in following analyses. The modified ICU is a 19-item
rest periods at the onset and conclusion of the physiological scale derived from the APSD to specifically assess callous-
recording.Forthepurposeofthecurrentstudy,psychophysi- unemotional behaviors associatedwithantisocialpersonality
ologicaldatafromthetworestperiodswereused.Monetary and has demonstratedconvergentvalidity with existing self-
compensationwasprovidedtoparticipatingfamiliesattheend and parent-report measures of psychopathic behaviors (Gao
oftheassessment.TheuniversityInstitutionalReviewBoard andZhang2016).Caregiversareaskedhowwellcertainstate-
approvedallprocedures,andbothparentalconsentandchild ments describe their child; e.g. BSeems very cold and
assentwereobtained. uncaring,^ and BIt is easy to tell how he/she is feeling.^
Itemsareratedona4-pointscale(0=notatalltrue,1=some-
Measures whattrue,2=verytrue,3=definitelytrue).Subscalescores
were derived by summing the raw scores from each item.
Child Behavior Checklist (CBCL; Achenbach and Cronbach’s α was 0.85, 0.71, 0.83, and 0.63 for the total
Rescorla 2001) Caregivers completed the CBCL, a rating ICU, callousness (7 items), uncaring (8 items), and unemo-
scalecomposedof112itemsconcerningthechild’sbehavior tionalsubscales(4items),respectively.
now or within the past 6 months; e.g. BArgues a lot,^ or
BImpulsiveoractswithoutthinking.^Itemsareratedona3- Diagnostic Interview Schedule for Children (DISC-IV;
point scale (0 = not true, 1 = sometimes or somewhat true, Shaffer et al. 2000) The trained research assistant adminis-
2=verytrueoroftentrue).TheCBCLhasdemonstratedboth tered the DISC-IV to caregivers, a structured interview that
validityandreliabilityforthe assessmentofchildpsychopa- assesses the lifetime number of conduct disorder (CD) and
thology(Dutraetal.2004).Forthepresentinvestigation,the oppositional defiant disorder (ODD) symptoms in children,
aggression and rule-breaking subscales were used (18 items e.g., if the child has everusedalcohol orbeensuspended or
and17items,respectively).Subscalescoreswerederivedby expelled from school. The DISC has shown validity for
summingtherawscoresfromeachitem.Cronbach’sαinthe assessing various psychopathologies in youth (Schwab-
JAbnormChildPsychol
Stone et al. 1996). Although none of the participants in our decomposed into separate component HRV frequencies using
samplemetthediagnosticcriteriaforCDorODD,44%ofthe Fast Fouriertransformation algorithms. Power in the high fre-
boyshadatleastoneCDsymptom,and22%ofboyshadat quency range (0.15–0.40 Hz; ms2), indexing parasympathetic
least2CDsymptomsintheirlifetime.Incontrast,only28%of activity(Berntsonetal.1997),wasusedinstatisticalanalysis.
girls had one ormoreCDsymptoms. ForODD,84% ofthe
boyshadatleastonesymptom,and75%ofboyshadatleast2
PEP PEP, an index of sympathetic-related cardiac activity
symptoms in their lifetime. In girls, 81% had one or more
(Berntson et al. 1994; Brenner and Beauchaine 2011), was
ODD symptoms. In the following analyses, ODD and CD
measured using the NICO100C and ECG100C amplifiers.
symptom counts were combined to create a variable called
Electrodes were configured according to previous research
BODD/CDSymptoms.^
(Sherwood et al. 1990). The QRS and dZ/dt B waveforms
wereensemble-averagedusingAcqKnowledge4.2.PEPwas
SocialAdversityAself-reportsocialadversityindexwascre-
measuredasthe time(ms)elapsed,between the onset ofthe
ated based on caregivers’ answers to questions defined in
Q-waveandtheimpedancedZ/dtB-point.
previous literature (Gao et al. 2010; Moffitt 1990). A total
adversityscorewascreatedbyadding1pointforeachofthe
StatisticalAnalyses
followingtenvariables:DivorcedParents(singleparentfam-
ily, remarriage, or living with guardians other than parents),
AllanalyseswereconductedusingSPSS22.0and23.0.Pearson
Foster Home, PublicHousing, WelfareFood Stamps, Parent
correlationswereconductedtoexaminetheassociationsamong
EverArrested(either parenthas beenarrestedatleast once),
study variables and independent samples t-tests to investigate
Parents Physically Ill, Parents Mentally Ill, Crowded Home
genderdifferences.Weperformedafactoranalysisoftheeight
(five or more family members per room within the home),
behavioral subscale measures (aggression, rule-breaking, CD/
Teenage Mother (aged 19 years or younger when child was
ODD symptoms, impulsivity, narcissism, unemotional behav-
born),andLargeFamily(havingfiveormoresiblingsbyage
ior,callousness,anduncaringbehavior)toreducethemeasures
3year).Allitemswereassessedfortheparticipants’lifetime
to a single comprehensive factor score for general antisocial
andwerescoredeither0(no)or1(yes),withahightotalscore
behavior. This factor score was then entered as the dependent
indicatinghighersocialadversity.
variableintoamoderatedmultiplemediationanalysisusingthe
PROCESSmacroforSPSS(Hayes2013),withsocialadversity
PsychophysiologicalDataAcquisitionandReduction
astheindependentvariable,thethreephysiologicalmeasuresas
parallelmediators,andgenderasamoderator.Figure1showsa
Psychophysiological data were collected continually using a
schemata of the moderated multiple mediation model (a
BIOPAC MP150 system (Biopac Inc., CA). HR, HRV, and
statistical representation of the model can be found in Hayes
PEPwereeachaveragedfromtheinitial2-minrestperiodat
2015,Fig.2PanelA).
theonsetofthecomputerizedtasksandthe2-minrestperiod
Specifically, we tested whether gender moderated the link
attheculminationofthecomputerizedtasks.Forsubjectswith
betweenANSmediatorsandantisocialbehavior.Amoderated,
unavailableorunsuitabledata(duetomovement)foreitherof
multiple mediator model allows investigators to evaluate the
thetworestperiods,weusedtheavailablerestperioddatafor
contributionofeachmediatorandmoderatorwhilecontrolling
thatparticipant(N=37).Childrenwereinstructedtositqui-
for other paths in the model (Duffy et al. 2012; Hayes2015).
etlyandrestduringtherestperiods.
ThePROCESSmacrocomputesthebootstrappedbiascorrected
HR HR was analyzed offline with Kubios HRV software
(Version 2.2; Tarvainen et al. 2014). Electrocardiography
(ECG) signal was recorded using ECG100C with two pre-
jelledAg-AgCldisposablevinylelectrodesplacedatamodi-
fied Lead II configuration. Research assistants cleaned the
contactareausing NuPrep™priortoaffixingtheelectrodes.
Allintervalswerevisuallyinspectedandcorrectedforfalseor
undetected R-waves, movement artifacts, and ectopic beats.
Heartratewasmeasuredinbeatsperminute(bpm),basedon
theaverageofinter-beatintervals(IBI;R-Rwaveintervals).
HRV ECG channel recording was analyzed offline using
Kubios HRV software (Version 2.2; Tarvainen et al. 2014).
Fig.1 Moderatedmultiplemediationmodeloftherelationshipbetween
AftervisuallyinspectingtheR-waves,theIBItimeserieswas socialadversityandantisocialbehavior
JAbnormChildPsychol
95%confidenceintervals(CI)oftheconditionalindirecteffects adversityandHRV,b=0.25,p<0.05,butnoassociationbe-
by taking 10,000 bootstrapped samples (Hayes 2013). tween social adversity and PEP, b = 2.93, p = 0.41. Gender
Confidence intervals of the conditional indirect effect that do moderatedtherelationshipbetweenHRandantisocialbehavior,
not contain zero indicate significant mediation effects. b=0.04,p<0.01,butnottherelationshipbetweenHRVand
Complete mediation occurs when path c’ (the direct effect) is antisocial behavior, b = 0.48, p = 0.12, or PEP and antisocial
equalto0,suggestingtheassociationbetweenXandYisfully behavior,b=0.00,p=0.57.HR,b=−0.08,p<0.01,andHRV,
accounted for by the mediators, and partial mediation occurs b=−0.98,p=0.05,significantlypredictedantisocialbehavior
whenpathc’isavalueotherthan0butsignificantlylessthan aftercontrollingfortheothervariablesinthemodel,thoughPEP
pathc(BaronandKenny1986).Weranadditionalmoderated didnot,b=−0.00,p=0.67.Thedirecteffectofsocialadversity
multiple mediation models substituting other behavioral out- onantisocialbehaviorremainedsignificant,b=0.75,p<0.01,
comes for general antisocial behavior. In order to rule out re- 95%CI=[0.32,1.19],suggestingpartialmediation.
versecausation,additionalmediationmodelswereconstructed Conditionalindirecteffectsshowedthattheindirecteffect
withtheindependentvariableassocialadversity,thedependent ofHRonthe relationship between socialadversity and anti-
variableasoneofthethreeANSmeasures,andthemediatoras social behavior was significant for males, b = 0.19, 95%
generalantisocialbehavior. CI = [0.02, 0.47], but not for females, b = 0.01, 95%
CI = [−0.09, 0.14]. Similarly, the conditional indirect effect
ofHRVontherelationshipbetweensocialadversityandanti-
Results social behavior was significant for males, b = −0.12, 95%
CI = [−0.35, −0.01], but not for females, b = −0.01, 95%
DescriptiveStatisticsandCorrelationalAnalyses CI=[−0.13,0.11].However,therewasnosignificantinterac-
tion effect between HRVand gender in the model, and the
Outliers beyond 3SDs above or below the means were re- index ofmoderated mediation was alsonot significant,95%
moved fromanalyses. Logarithmic transformationswereap- CI=[−0.02,0.41],suggestinggenderdidnotactuallymoder-
pliedtoHRV,rule-breakingbehavior,aggression,externaliz- ate the indirect effect of HRVon the relationship between
ing(total),ODD/CDsymptoms,callousness,narcissism,and socialadversityandantisocialbehavior.PEPdidnotmediate
socialadversitypriortofurtheranalysestoreduceskewness. therelationshipbetweensocialadversityandantisocialbehav-
The single factor solution of the eight behavioral measures ior,norwasthereamoderatingeffectofgender(allcondition-
wasstandardizedusingtheAnderson-Rubinmethod(M=0, alindirecteffectsns).SeeTable3formodelsresults.1,2
SD=1).Thisgeneralantisocialbehaviorfactoraccountedfor Exploratoryanalyseswereconductedtopredicteachanti-
approximately52%ofthevariance(Eigenvalue=4.134)with socialmeasure.The conditionalindirecteffectof HRon the
factorloadingsrangingfrom0.455forunemotionalbehavior relationshipbetweensocialadversitywassignificantformales
to0.819foraggression. forexternalizing,b=0.07,95%CI=[0.01,0.16],aggression,
Malesandfemalesdifferedsignificantlyonbothbehavioral b = 0.08, 95% CI = [0.01, 0.18], narcissism, b = 0.05,
measuresandphysiologicalmeasures.Means,standarddevi- CI = [0.01, 0.12], uncaring behavior, b = 0.62, 95%
ations, and group comparisons of all variables are listed in CI = [0.05, 1.72], and callous-unemotional traits (ICU total
Table 1. In males, social adversity was positively associated score),b=0.85,95%CI=[0.02,2.54],butnotforfemales(all
withgeneralantisocialbehavior,ODD/CDsymptoms,narcis- conditionalindirecteffectsns).3
sism,andimpulsivity,andHRV.Asexpected,HRwasnega- Finally,reverse-causalityanalysesshowedthatgeneralan-
tivelyassociatedwithgeneralantisocialbehavior,externaliz- tisocial behavior marginally mediated the relationship
ing,aggression,rule-breaking,ICUtotalscore,anduncaring
behavior.Infemales,socialadversitywaspositivelyassociat-
edwithgeneralantisocialbehavior,externalizing,aggression,
rule-breaking,andnarcissism,butneitherHRnorHRVwere 1Moderatedmultiplemediationanalyseswerealsoconductedusingacom-
associated with behavioral measures. In both males and fe- positescoreofantisocialbehavior,derivedfromsummingthesubscalescores
(externalizingbehavior,ODD/CDsymptoms,narcissism,impulsivity,and
males, PEP was not linked to any of the antisocial behavior
callous-unemotionalbehavior)inordertomaintainconsistencyandcompara-
outcomesnorsocialadversity.Correlationsorganizedbygen- bilitywithChoyetal.(2015).Resultswerethesameusingthecomposite
der are presented in Table 2, and were substantively un- score.
changedwhencontrollingforethnicity. 2TheSPSSPROCESSmacrowhichusesbootstrappedconfidenceintervalsto
indexmoderatedmediationisalsorobusttohighlyskewedrawdata(Hayes
2015).
ModeratedMultipleMediationAnalyses 3Exploratoryanalyseswerealsoconductedwithastandardizedantisocial
behaviorfactorscore.Afactorscoreforantisocialbehaviorwasconstructed
fromstandardizedvaluesofeachsubscalemeasureandenteredasadependent
Bootstrapping analyses revealed a direct association between
variableinthemoderatedmultiplemediationmodel.Allresultsweresubstan-
social adversity and HR, b = −4.61, p < 0.05, and social tivelythesame.
JAbnormChildPsychol
Table1 Descriptivestatistics
Measure Males Females Genderdifferences
Mean(SD) Min Max Mean(SD) Min Max t df
HR 85.13(10.06) 61.15 113.75 88.24(10.22) 65.41 117.96 -2.78** 328
HRVa 3.22(0.50) 1.79 4.28 3.23(0.44) 1.99 4.23 -0.21 329
PEP 84.38(16.94) 39.00 132.50 82.28(14.21) 40.00 120.00 1.22 327
GeneralAntisocialBehavior 0.14(1.03) -1.73 3.03 -0.13(0.96) -1.65 2.54 2.46* 312
ExternalizingBehaviora 7.29(6.75) 0 30 5.81(5.89) 0 27 2.25* 334
Aggressiona 5.17(5.24) 0 25 4.11(4.33) 0 21 1.96* 335
Rule-BreakingBehaviora 2.23(2.15) 0 14 1.71(1.96) 0 9 2.65** 334
ODD/CDa 5.24(4.11) 0 19 3.98(3.61) 0 15 2.77** 328
Narcissisma 2.00(2.12) 0 12 1.75(1.90) 0 9 1.20 328
Impulsivity 2.77(1.80) 0 8 2.45(1.71) 0 8 1.66 328
ICU 15.75(7.65) 0 38 14.61(7.95) 0 36 1.33 332
Callousnessa 2.04(2.36) 0 13 1.84(2.56) 0 15 1.48 332
Uncaring 9.69(4.90) 0 24 9.09(5.05) 0 21 1.10 332
Unemotional 4.02(2.25) 0 10 3.68(2.41) 0 10 1.31 332
SocialAdversitya 3.05(2.07) 0 10 2.91(2.01) 0 8 0.58 332
Descriptivestatisticsshowuntransformedvalues;standarddeviationsappearinparenthesesnexttomeans;independentsamplest-testsconductedon
transformedvalues(a)formalesandfemales;boldfacetypedenotessignificantdifferencebetweenmalesandfemales
HRheartrate,HRVheartratevariability,PEPpre-ejectionperiod,ODD/CDOppositionalDefiantDisorder/ConductDisorder,ICUInventoryofCallous-
UnemotionalTraits
**p≤0.01,*p≤0.05,two-tailed
betweensocialadversity and HR (indirect effect: b = −1.14, Discussion
SE = 0.61, 95% CI = [−2.77, −0.25]). Normal theory tests
revealed the indirect effect to be marginally significant, ThisstudyexaminedthemediatingeffectsofANSactivityon
p=0.05,withasmalleffectsize,κ2=0.031.Wethentested therelationshipbetweensocialadversityandantisocialbehav-
thismodel withgendermoderatingthe linkbetween general iorinchildren.Wefoundthatinmales,lowrestingHRmedi-
antisocialbehaviorandHR,butfoundnoevidenceofmoder- ated the relationship between social adversity and antisocial
ated mediation. Lastly, general antisocial behavior did not behaviors.AlthoughHRV,anindicatorofparasympatheticac-
mediate the relationship between social adversity and HRV, tivity,wasrelatedtosocialadversityinmales,itwasnotrelated
norbetweensocialadversityandPEP(allindirecteffectsns). to any of the antisocial measures, nor did it mediate the
Table2 Correlationsbygender
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
1 HR 1 -0.59** -0.15 -0.05 -0.08 -0.05 -0.11 -0.02 0.08 -0.02 0.02 .00 0.02 -0.04 -0.09
2 HRVa -0.71** 1 0.05 0.01 0.09 0.04 0.12 -0.01 -0.08 -0.03 0.02 -0.01 0.05 -0.03 0.11
3 PEP -0.13 0.08 1 0.04 -0.03 -0.03 -0.03 -0.10 0.09 0.08 0.05 0.02 0.06 0.05 -0.04
4 GeneralAntisocialBehavior -0.25** 0.04 0.06 1 0.84** 0.81** 0.78** 0.60** 0.77** 0.75** 0.78** 0.69** 0.70** 0.44** 0.18*
5 Externalizinga -0.23** 0.09 0.04 0.86** 1 0.96** 0.83** 0.55** 0.62** 0.62** 0.48** 0.46** 0.45** 0.22** 0.22**
6 Aggressiona -0.27** 0.11 0.06 0.83** 0.96** 1 0.68** 0.57** 0.60** 0.59** 0.46** 0.44** 0.42** 0.23** 0.21**
7 Rule-BreakingBehaviora -0.19* 0.11 0.05 0.80** 0.85** 0.71** 1 0.44** 0.54** 0.52** 0.48** 0.48** 0.45** 0.18* 0.24**
8 ODD/CDa -0.13 0.01 -0.04 0.58** 0.45** 0.48** 0.31** 1 0.39** 0.38** 0.35** 0.38** 0.31** 0.17* 0.13
9 Narcissisma -0.14 -0.02 0.07 0.80** 0.66** 0.63** 0.65** 0.37** 1 0.54** 0.48** 0.40** 0.46** 0.24** 0.20*
10 Impulsivity -0.05 -0.08 0.07 0.80** 0.61** 0.59** 0.57** 0.39** 0.67** 1 0.47** 0.47** 0.45** 0.19* 0.13
11 ICUtotal -0.18* 0.11 0.04 0.79** 0.52** 0.51** 0.52** 0.35** 0.46** 0.49** 1 0.71** 0.92** 0.65** 0.07
12 Callousnessa -0.14 0.12 -0.02 0.70** 0.53** 0.53** 0.49** 0.32** 0.52** 0.55** 0.62** 1 0.54** 0.22** 0.11
13 Uncaring -0.17* 0.05 0.06 0.68** 0.45** 0.45** 0.44** 0.38** 0.39** 0.40** 0.91** 0.38** 1 0.45** 0.07
14 Unemotional -0.09 0.12 0.05 0.46** 0.24** 0.21** 0.30** 0.06 0.15 0.24** 0.74** 0.31** 0.53** 1 0.02
15 SocialAdversitya -0.15 0.16* 0.11 0.20* 0.09 0.09 0.12 0.19* 0.18* 0.20* 0.06 0.02 0.08 0.00 1
AreaabovediagonalshowsPearson’scorrelationsforfemales,areabelowthediagonalshowsPearson’scorrelationsformales
HRheartrate,HRVheartratevariability,PEPpre-ejectionperiod,ODD/CDOppositionalDefiantDisorder/ConductDisorder,ICUInventoryofCallous-
UnemotionalTraits
aLog-transformedvariables
**p≤0.01,*p≤0.05,two-tailed
JAbnormChildPsychol
Table3 Moderatedmultiple
mediation:Indirecteffectof VariableModel(n=298)
SocialAdversity(X)onGeneral Outcome Predictor B SE t-Value p-Value
AntisocialBehavior(Y)through
Independentvariabletomediator
AutonomicNervousSystem
ANS
measures(M)asmoderatedby
Gender(V) HR(M1) SA -4.606 2.185 -2.108 0.036*
HRV(M) SA 0.246 0.104 2.370 0.018*
2
PEP(M) SA 2.932 3.665 0.800 0.424
3
Mediatortodependentvariable
GeneralAntisocialBehavior
HR -0.079 0.024 -3.268 0.001**
HRV -0.975 0.497 -1.960 0.051
PEP -0.005 0.011 -0.427 0.670
Gender -5.460 2.199 -2.483 0.014*
HRxGender 0.039 0.015 2.657 0.008*
HRVxGender 0.478 0.309 1.545 0.123
PEPxGender 0.004 0.007 0.567 0.571
SA 0.754 0.220 3.432 0.001**
DirectEffectofXonY
B SE t-Value p-Value 95%CI
0.754 0.220 3.432 0.001* [0.322,1.187]
ConditionalIndirectEffectsatEachLeveloftheModerator
Males Females
Mediator B SE 95%CI B SE 95%CI
HR 0.185 0.112 [0.023,0.474] 0.006 0.052 [−0.087,0.135]
HRV -0.122 0.084 [−0.351,−0.009] -0.005 0.060 [−0.131,0.114]
PEP -0.002 0.020 [−0.059,0.028] 0.011 0.029 [−0.019,0.122]
IndexofModeratedMediation
Mediator Index SE 95%CI
HR -0.179 0.121 [−0.515,−0.017]
HRV 0.117 0.104 [−0.016,0.408]
PEP 0.012 0.035 [−0.026,0.142]
Bootstrapsamples=10,000.Boldfacetypedenotessignificantmediationeffect
Bunstandardizedregressioncoefficients,SEstandarderror,SAsocialadversity,ANSautonomicnervoussystem,
HRheartrate,HRVheartratevariability,PEPpre-ejectionperiod
**p≤0.01*p≤0.05,two-tailed
relationship between social adversity and antisocial behavior. coinhibition,coactivation,andindependently-mediatedactivity
Whilesocialadversitywasstronglyrelatedtofemaleantisocial ispossible.Theinvestigationintotheseparableinfluencesofthe
behavior,restingHRorHRVwasnot.Finally,PEP,anindica- sympathetic and parasympathetic nervous systems provides a
torofsympatheticactivity,wasnotrelatedtoanyoftheantiso- scientificallyvaluableandnovelcontributiontodevelopmental
cial measures and did not mediate the relationship between researchonantisocialbehavior.Specifically,thenullmediating
socialadversityandantisocialbehaviorineithergendergroup. effects of the sympathetic and parasympathetic measures sug-
Toourknowledge,thiswasthefirstinvestigationaimingto gestthatcontrarytocommontheoreticalassumption,themech-
tease apart parasympathetic from sympathetic influences on anism underlying low resting heart rate cannot be reduced to
resting HR in the context of ANS mediation between social sympatheticunderarousal.
adversity and antisocial behavior. We found that neither PEP Our hypotheses were partially supported. The moderat-
nor HRV were mediators, suggesting that neither sympathetic ed multiple mediation model showed that resting HR me-
norparasympatheticactivityaloneisresponsiblefortheunique diated the relationship between social adversity and gen-
wayinwhichHRinfluencesantisocialbehavior.Whileboththe eral antisocial behavior (as well as externalizing, aggres-
sympatheticandparasympatheticsystemsaffectHR,theirrela- sion, narcissism, uncaring behavior and callous-
tionship to one another is not necessarily related, and as such unemotional traits) in males only. As evidenced by a
JAbnormChildPsychol
non-zero indirect effect, low resting HR was a mechanism 2011).Thesesexdifferencesbecomemorepronouncedatthe
through which social adversity exerted its influence on transitionfrommiddlechildhoodtoadolescence(DelGiudice
antisocial behavior (Table 3) (Hayes 2009). These results etal.2011),whichencapsulatesourpopulationsample.
parallel Choy et al. (2015)‘s finding that HR during a Wecannotruleoutthepossibilitythattherelationshipbe-
stressor task mediates the relationship between antisocial tweensocialadversityandantisocialbehaviorinfemalesdoes
behavior and social adversity in 11 to 12 year olds. not operate mechanistically through cardiovascular changes,
Together, this supports the theoretical accounts that social thoughitmaybereflectedinothermeasuresofANSactivity
adversity leads to a state of blunted arousal (Lovallo et al. such as skin conductance (Beauchaine et al. 2008). In addi-
2012), which may then promote antisocial behavior, per tion, current measures of antisocial behavior tend to ignore
the fearlessness and sensation seeking theories. This in- relational aggression, which is commonly displayed in girls
formation is clinically relevant and has implications for withantisocialbehavior(CrickandGrotpeter1995).Hadre-
shaping public policy and community-related program- lational aggression been included we may have seen a rela-
ming. While we do not directly address the extent to tionship between ANS measures and antisocial behavior in
which HR-mediated antisocial behavior in males is due girls.Relationalaggressionwasrelatedtobluntedphysiolog-
to sensation seeking or fearlessness, activities that have ical responding in maltreated and nonmaltreated children
the potential to mirror the physiological arousal gained (Murray-Closeetal.2008)aswellasinfemaleswithahistory
from antisocial behavioral demonstrations, such as orga- ofsexualabuse(Murray-CloseandRellini2012).Futurestud-
nized sports and other Bthrill-seeking^ recreational activ- iesshouldincorporaterelationalaggressionintoacomposite
ities, could be used to supplement arousal levels in males. measureofantisocialbehaviortoaddressthisissue.
OursamplewasyoungerthanthatofChoyetal.(2015)‘s. Oneofthelimitationsisthatweofferonlyacross-sectional
Theoreticalaccountsofantisocialbehaviorsuggesttwoalter- viewofantisocialbehavior.Futuredirectionsshouldincludea
natepathways:life-coursepersistentandadolescence-limited. longitudinalperspective thatlooks atthe stability ofthe me-
Because our sample is notably pre-adolescent (7–10 years diatoreffectovertime(SeligandPreacher2009).Thoughwe
old), our results offer insight into components that may be could not conclusively rule out reverse-causation (we found
more relevant to life-course persistent rather than thatantisocial behaviormarginally mediatedthe relationship
adolescence-limited antisocial behavior. Ifthe ANS issensi- betweensocialadversity and heart rate),thismodel was sta-
tivetoenvironmentalchanges,theeffectsofpersistentadver- tistically weak and is theoretically unlikely, given the cross-
sityshouldbecumulative,makingearlyinterventioncritical, sectionalnatureofthedata.Second,oursocialadversitymea-
given that life-course persistent antisocial behavior is stable suredoesnotaccountforotherpsychosocialinfluencessuch
acrossdevelopment(MoffittandCaspi2001). aspeerinfluenceorneighborhoodcrimestatistics.Third,sev-
Socialadversityremainedarobustcorrelateofgeneralan- eralbehavioralmeasureshaverelativelylowlevelsofreliabil-
tisocialbehaviorforgirls,specificallyexternalizingbehaviors ityandcombiningthemmayleadtolowerreliability,therefore
and psychopathic-like narcissism, though HR did not. we suggest cautious interpretation of the results. However,
AlthoughChoyetal.(2015)foundunchangedmediationef- previousstudieshaveshowncomparablealphalevelsforboth
fectscontrollingforgender,theydidnotexaminetheseeffects theunemotionalsubscaleoftheICU(Essauetal.2006)and
for males and females separately. Our results are consistent the impulsivity subscale of the APSD (Lynam 2006; Ross
with recent research that suggests that in normative popula- etal.2007).Lastly,oursampleispredominantlylow-income,
tions,thebluntedANSrespondingcharacteristicofantisocial thereforetheseresultsmaynotbeasreadilygeneralizableto
behavior and psychopathy is more prevalent in boys rather the broader population. Regardless, our results contribute to
than in girls (Beauchaine et al. 2008), and that the develop- the growing body of knowledge concerning the mediating
mentand display ofantisocialbehavioringirlscomparedto effectsofbiologicalprocessesonthelinkbetweensocialad-
boysisaresultofincreasedsusceptibilitytosocialandenvi- versityandantisocialbehavior.Itisimportanttofollowupon
ronmentalinfluences(Beauchaineetal.2008).Alternatively, thediscrepanciesthatwesawbetweenmalesandfemalesas
ifsocialstressorsandenvironmentaladversitydoalterphys- concerns physiological arousal and antisocial behavior.
iologyinfemales,thesephysiologicalchangesmaybedistinct Accumulating evidence suggests that there are meaningful
fromthoseofmalesandmanifestinalternatebehavioralout- differencesbetweenmalesandfemalesregardingtheetiology
comes. The Adaptive Calibration Model hypothesizes that anddevelopmentalcoursesofantisocialbehavior.
extremestressdesensitizestheautonomicresponseinmales,
promotingantisocialbehaviorandelevatedrisk-takingthatis Acknowledgements ThisstudywassupportedbytheEuniceKennedy
evolutionarilyadaptive;infemales,however,increasedstress ShriverNationalInstituteofChildHealth&HumanDevelopmentofthe
National Institutes of Health to Yu Gao under Award Number
can result in increased responsivity, an adaptive mechanism
SC2HD076044.The contentissolelythe responsibility ofthe authors
thatultimatelypromotesrapidadaptationtothechangingen-
and does not necessarily represent the official views of the National
vironmentsuchthatfertilityismaximized(DelGiudiceetal. InstitutesofHealth.WewouldliketothankthePsychophysiologyLab
JAbnormChildPsychol
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