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NEW RESEARCH Mediation of Sensation Seeking and Behavioral Inhibition on the Relationship Between Heart Rate and Antisocial Behavior: The TRAILS Study Jelle J. Sijtsema, MSc., René Veenstra, Ph.D., Siegwart Lindenberg, Ph.D., Arie M. van Roon, Ph.D., Frank C. Verhulst, M.D., Ph.D., Johan Ormel, Ph.D., Harriëtte Riese, Ph.D. Objective: Why is low resting heart rate (HR) associated with antisocial behavior (ASB), i.e., aggression and rule breaking, in adolescence? Theory suggests that personality traits mediate this relationship but differently with age. In the present study this age-effect hypothesis is tested; we expected that the relationship between HR and aggression would be mediated in preadolescence by the personality trait behavioral inhibition, but not by sensation seeking. However, the relationship between HR and rule breaking in adolescence was predicted to be mediated by sensation seeking, but not by behavioral inhibition. Hypotheses were tested separately for boys and girls. Method: HR in supine position was assessed in repondents to the TRacking Adolescents’ Individual Lives Survey (TRAILS) (N 1,752; 48.5% boys) at age 11 years. Rule breaking and aggression at age 16 were assessed with two subscales from the Youth Self Report (YSR) questionnaire. Personality (i.e., sensation seeking and behavioral inhibition) was measured at ages 11, 13.5, and 16 with the Early Adolescent Temperament Questionnaire–Revised (EATQ-R), Behavioral Inhibition System/ Behavioral Activation Sys- tem (BIS/BAS) scales, or NEO Personality-Index Revised (NEO-PI-R). Results: In boys, lower HR was associated with aggression and rule breaking in adolescence. The association between HR and rule breaking was mediated by sensation seeking in adolescence but not in preadolescence. Girls’ HR was not associated with ASB, and no mediating effects were found. Conclusions: Our findings support the age-effect hypothesis in boys’ rule breaking behavior. This shows that the association between HR and ASB depends on age, gender, and subtype of ASB. J. Am. Acad. Child Adolesc. Psychiatry, 2010;49(5):493–502. Key Words: heart rate, rule breaking, aggression, gender L ow heart rate (HR) is one of the strongest and most often replicated physiological cor- relates of antisocial behavior (ASB) in child- hood and adolescence. 1 However, longitudinal studies focusing on developmental pathways and studies on the relationship of HR to subtypes of ASB (i.e., aggression, rule breaking) are still lacking. 2,3 Often, two theoretical explanations for the relationship between HR and ASB are given. 4 According to the stimulation-seeking theory, some adolescents are constantly underaroused, which is presumably marked by a low HR and a subjective unpleasant state. 4-6 Behaving antiso- cially is assumed to increase HR and to be accompanied by a more comfortable state. Alter- natively, in the fearlessness theory, a general lack of anxiety and inhibition is assumed to be re- quired to conduct ASB. 5,7 Despite their differ- ences, both theories suggest that the relationship between HR and ASB may be mediated by per- sonality traits. Before we focus on these mediation factors, we take a closer look at the established relationship between HR and ASB. 1,5,8 Previous studies typi- cally focused on one type of ASB or used ASB as This article is discussed in an editorial by Dr. David C. Rettew on page 441. JOURNAL OF THE AMERICAN ACADEMY OF CHILD & ADOLESCENT PSYCHIATRY VOLUME 49 NUMBER 5 MAY 2010 493 www.jaacap.org

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NEW RESEARCH

Mediation of Sensation Seeking andBehavioral Inhibition on the Relationship

Between Heart Rate and AntisocialBehavior: The TRAILS Study

Jelle J. Sijtsema, MSc., René Veenstra, Ph.D., Siegwart Lindenberg, Ph.D.,Arie M. van Roon, Ph.D., Frank C. Verhulst, M.D., Ph.D., Johan Ormel, Ph.D.,

Harriëtte Riese, Ph.D.

Objective: Why is low resting heart rate (HR) associated with antisocial behavior (ASB), i.e.,aggression and rule breaking, in adolescence? Theory suggests that personality traits mediatethis relationship but differently with age. In the present study this age-effect hypothesis istested; we expected that the relationship between HR and aggression would be mediated inpreadolescence by the personality trait behavioral inhibition, but not by sensation seeking.However, the relationship between HR and rule breaking in adolescence was predicted to bemediated by sensation seeking, but not by behavioral inhibition. Hypotheses were testedseparately for boys and girls. Method: HR in supine position was assessed in repondents tothe TRacking Adolescents’ Individual Lives Survey (TRAILS) (N � 1,752; 48.5% boys) at age11 years. Rule breaking and aggression at age 16 were assessed with two subscales from theYouth Self Report (YSR) questionnaire. Personality (i.e., sensation seeking and behavioralinhibition) was measured at ages 11, 13.5, and 16 with the Early Adolescent TemperamentQuestionnaire–Revised (EATQ-R), Behavioral Inhibition System/ Behavioral Activation Sys-tem (BIS/BAS) scales, or NEO Personality-Index Revised (NEO-PI-R). Results: In boys,lower HR was associated with aggression and rule breaking in adolescence. The associationbetween HR and rule breaking was mediated by sensation seeking in adolescence but not inpreadolescence. Girls’ HR was not associated with ASB, and no mediating effects werefound. Conclusions: Our findings support the age-effect hypothesis in boys’ rule breakingbehavior. This shows that the association between HR and ASB depends on age, gender, andsubtype of ASB. J. Am. Acad. Child Adolesc. Psychiatry, 2010;49(5):493–502. Key Words: heartrate, rule breaking, aggression, gender

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L ow heart rate (HR) is one of the strongestand most often replicated physiological cor-relates of antisocial behavior (ASB) in child-

hood and adolescence.1 However, longitudinalstudies focusing on developmental pathwaysand studies on the relationship of HR to subtypesof ASB (i.e., aggression, rule breaking) are stilllacking.2,3 Often, two theoretical explanations forthe relationship between HR and ASB are given.4

According to the stimulation-seeking theory,

This article is discussed in an editorial by Dr. David C. Rettew on

cpage 441.

JOURNAL OF THE AMERICAN ACADEMY OF CHILD & ADOLESCENT PSYCHIATRY

VOLUME 49 NUMBER 5 MAY 2010

ome adolescents are constantly underaroused,hich is presumably marked by a low HR and a

ubjective unpleasant state.4-6 Behaving antiso-ially is assumed to increase HR and to beccompanied by a more comfortable state. Alter-atively, in the fearlessness theory, a general lackf anxiety and inhibition is assumed to be re-uired to conduct ASB.5,7 Despite their differ-nces, both theories suggest that the relationshipetween HR and ASB may be mediated by per-onality traits.

Before we focus on these mediation factors, weake a closer look at the established relationshipetween HR and ASB.1,5,8 Previous studies typi-

ally focused on one type of ASB or used ASB as

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an aggregate measure of rule-breaking and ag-gressive behavior. There are a few notable excep-tions showing that a distinction of subtypes ofASB may be useful,9,10 and aggression and rulebreaking have been shown to be distinct, al-though correlated, subtypes of ASB.11 To con-sider a mediation model, we lean on previousfindings on the relationships between “HR andpersonality” and “personality and ASB.” Lowresting HR has been associated with high levelsof impulsivity or low levels of inhibition andwith high levels of sensation and novelty seekingin adolescents and adults.12-14 Previous studieson the relationship between personality and ASBshow that both low inhibition and sensationseeking have been linked to aggression and rule-breaking.15 Likewise, low inhibition in childhoodhas been shown to lead to rule-breaking in ado-lescence and to aggression in general.16,17 Effortsto distinguish between these two personalitytraits have been hampered by conceptual andmeasurement overlap, making it thus impossibleto tap into the different relationship of HR withsensation seeking and behavioral inhibition andthe different contribution of personality traits onaggression and rule breaking.

In the present study we assessed whether thepersonality traits “sensation seeking” and “lowbehavioral inhibition” could mediate the rela-tionship between HR and ASB. In addition, weconsidered the possibility that both “sensationseeking” and “fearlessness” theories are true, butfor different age groups and subtypes of ASB.This has not been tested before, but is inspired byprevious research showing distinct developmen-tal pathways for rule breaking and (physical)aggression. Incidences of rule breaking rise inadolescence, with a peak of offending in middleadolescence,18 whereas physical forms of aggres-sion are relatively frequent in childhood butsteadily decline in adolescence. These findings onASB seem in accordance with the developmentalpathways of personality traits, as children havelower behavioral inhibition compared with ado-lescents and adults.19 Sensation seeking, how-ever, shows a rise from the beginning of adoles-cence, with a peak at the age of 15 to 16 years.Behavioral inhibition may thus be more linked toaggression, and sensation seeking more to rulebreaking.

How then is this age effect related to HR? Inline with the fearlessness theory, low HR may be

associated with low inhibition in preadolescents, a

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hich in turn is linked to aggression. However,n adolescence, low HR may be associated withoth sensation seeking and rule breaking but, tour knowledge, not with aggression and behav-

oral inhibition. From recent brain research, welso know that children who were low on behav-oral inhibition become high on sensation seekingater in life.20 This development in personalityould imply that those who are characterized byow HR are less inhibited in preadolescence andre likely the ones who are characterized by highensation seeking in adolescence, which in turn ishen related differently to aggression and rulereaking. To address these differences in devel-pmental pathways, we tested an age-effect hy-othesis in the present study. More precisely, wexpected (a) that behavioral inhibition in pread-lescence, but not in adolescence, mediates theelationship between HR and aggression. On thether hand, we expected (b) sensation seeking indolescence, but not in preadolescence, to medi-te the relationship between HR and rule break-ng.

If at all, previous studies focused only onross-sectional associations between HR and ASBnd HR and personality traits (with a few longi-udinal exceptions7,9,21,22). Moreover, samples in

hich HR was measured were typically smallnd comprised mostly clinical cases. To over-ome these limitations, we tested the mediationodels longitudinally, in a large population-

ased sample. In addition, we assessed person-lity at three different ages during preadoles-ence and adolescence (i.e., age 11, 13.5, and 16ears) and in three different ways, to increase theeneralizability and robustness of the findings.e formulated no specific hypotheses regarding

ender differences. However, previous studieshowed that girls have higher HR in general,2,22

hereas boys score in general higher on aggres-ion and rule breaking.23,24 Hence, we tested theediating role of sensation seeking and behav-

oral inhibition on the relation between restingR and rule breaking and aggressive behavior in

dolescence separately for boys and girls.

ETHODarticipantsata were collected in a general population of TRack-

ng Adolescents’ Individual Lives Survey (TRAILS), aarge prospective population study of Dutch adoles-ents with bi- or triennial measurements from age 11 to

t least age 25 (see Huisman et al. 25 for a full

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description of the sample). Parental informed consentwas obtained after the procedures had been fullyexplained. Detailed information about sample selec-tion and analysis of nonresponse bias has been re-ported elsewhere.26 The three assessment waves ranfrom March 2001 to July 2002 (T1), September 2003 toDecember 2004 (T2), and September 2005 to December2007 (T3). At T1, 2230 children (mean age � 11.09years, SD � 0.56 year) enrolled in the study of whom2149 (96.4%; mean age 13.56 years, SD � 0.53 year)participated at T2 and 1816 (81.4%; mean age 16.27years, SD � 0.73 year) at T3.

MeasuresAggression and Rule Breaking Behavior. The ASBsubtypes aggression and rule breaking behavior wereassessed as self-reported measures as part of thebroadband Youth Self Report (YSR) at age 16 years.27

The YSR covers behavioral and emotional problems inthe past 6 months. Good reliability and validity of theAmerican version were confirmed for the Dutch ver-sion.28 The rule breaking subscale consisted of 15 items(� � .76) assessing behaviors such as rule-breaking,truancy, and stealing. The adapted aggression subscaleconsisted of eight items (� � .71) assessing physicalacts against persons or things (i.e., fighting, being cruelto others). Subjects responded on a three-point scale (0� true, 1 � somewhat true, 2 � very often or true).Heart Rate. At age 11 years, cardiac autonomic func-tion was assessed by a three-lead electrocardiogramwhile participants were in supine position and breath-ing spontaneously. Dedicated software ([pre-]CARS-PAN, previously used, e.g., in Dietrich et al.29) wasused to detect R-peaks, to check signal stationarity, tocorrect for artifacts, and to calculate the interbeatinterval (IBI; in milliseconds) between two heartbeats.IBI is inversely related to HR by the equation HR �60,000/IBI. HR was expressed in beats per minute(bpm). Blocks were considered invalid if they con-tained artifacts with a duration of more than 5 seconds,if the total artifact duration was more than 10% of theregistration, or if the block length was less than 100seconds. Heart rate recordings were missing (n � 76)because of recording failure (41%) or signal analysisfailure (59%).Sensation Seeking and Behavioral Inhibition. Person-ality traits sensation seeking and behavioral inhibi-tion were assessed at age 11 with two subscales ofthe parent-reported Early Adolescent TemperamentQuestionnaire Revised (EATQ-R).30 Scales were con-structed based on a previous TRAILS studies.31

Sensation seeking was assessed with the high-inten-sity pleasure/surgency subscale, consisting of sixitems (� � .77) such as, “my child would find itexciting to travel to e.g., India or Africa” and “mychild would fear the thought of skiing down a steep

hill at high speed (reversely coded).” Behavioral w

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nhibition was assessed with the effortful controlubscale, consisting of eleven items (e.g., “my childnds it easy to focus on a task”; “is usually able totick with her/his plans and goals”) with goodnternal consistency (� � .86). Subjects responded onfive-point scale (1 � almost never true, 5 � almost

lways true).At age 13.5 years, the Behavioral Inhibition Sys-

em/ Behavioral Activation System (BIS/BAS) scalesere used to measure behavioral inhibition and

ensation seeking.32 Behavioral inhibition (BIS) wasssessed with seven items (� � 0.68), such as “Iorry about making mistakes” and “I have very few

ears compared to my friends [reversely coded].”ensation seeking was assessed with the four-itemun seeking subscale (� � 0.44), comprising itemsuch as “I crave excitement and new sensations” andI will often do things for no other reason than thathey might be fun.” Subjects responded on a four-oint scale (1 � untrue, 2 � somewhat untrue, 3 �omewhat true, 4 � true).

At age 16 years, we assessed behavioral inhibitionnd sensation seeking as part of the self-reportedevised Neuroticism-Extroversion-Openness Per-onality-Inventory (NEO-PI R).33 Behavioral inhibi-ion was measured with six items of the impulsivityubscale (� � 0.57; e.g., “I find it difficult to resistemptations” and “I can always control my feelingsreversely coded]”), after dropping two items be-ause of low internal consistency. Sensation seekingas assessed with the adventurism subscale, com-rising seven items (� � 0.59), such as “I hunger forxcitement” and “I like the thrill of the roller-oaster.” One item (“I like to wear clothes thattand-out or are colorful”) was dropped from theriginal subscale because of low internal consis-ency. Item scores ranged from 1 (fully disagree) to

(fully agree).

ata Analysisirst, summary statistics were given by calculatingeans (SD) of the study variables. Second, to test ourediation hypotheses, we computed linear regressionodels using one-tailed tests. Rule breaking and ag-

ression scores were logarithmically transformed toorrect for skewness (i.e., many participants scoredero on the scale). After transformation, both variablesere still skewed but considerably less.To test mediation properly,34 we tested first

hether there was a direct association of HR with ASBi.e., rule breaking or aggression). Furthermore, weested the association of HR with personality. Finally,

e tested whether the association between HR on ASBas mediated. Evidence for complete mediation is

iven when the direct association between HR andSB becomes zero, while allowing personality to me-iate this relationship. Partial mediation is applicable

hen this direct association becomes significantly

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lower. To test whether mediation was significant, weapplied the conservative Sobel test as well as a boot-strap approach,35 which enabled us to calculate the95% confidence intervals of the mediation effect. Boot-strapping generates k random samples (k is here 1,000)from the original distribution. This process yields kestimates of the indirect effect, which serve as empir-ical, nonparametric approximations of the samplingdistributions and thereby allow for non-normal multi-variate distributions in the data. Macros for this pro-cedure were downloaded from http://www.comm.o-hio-state.edu/ahayes. Regression analyses wereconducted separately per mediator and gender.

RESULTSSummary StatisticsTable 1 shows means, standard deviations, andgender differences of the study variables. Boysand girls differed significantly on almost allvariables. Supine HR at age 11 years was 3 to 4bpm higher in girls. Boys scored higher on rulebreaking and aggression at age 16 . Regardingpersonality traits, girls were higher than boys oneffortful control at age 11 and behavioral inhibi-tion at age 13.5, and scored higher on impulsivityat age 16. Boys scored higher on surgency andadventurism, at age 11 and 16 respectively.

HR and ASB: EATQ-RRegression analyses were conducted to study the

TABLE 1 Heart Rate, Antisocial Behavior, and Personalitand Gender Differences

Girls

N Mean SD

Age 11 yearsHeart rate (bpm) 902 78.72 11.05Effortful control (EATQ-R) 829 3.35 0.65Surgency (EATQ-R) 824 3.18 0.94

Age 13.5 yearsBehavioral inhibition (BIS) 858 2.66 0.51Fun-seeking (BAS) 858 2.67 0.48

Age 16 yearsAggression (YSR) 714 0.10 0.13Rule breaking (YSR) 715 0.24 0.17Impulsivity (NEO-PI-R) 713 2.87 0.55Adventurism (NEO-PI-R) 713 3.50 0.55

Note: Independent-samples t tests were used to calculate mean differencesInhibition Scale, bpm � beats per minute; EATQ-R � Early AdoleExtroversion-Openness Personality Inventory–Revised; YSR � Youth Sel

prospective relations between HR at age 11 and M

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ule breaking at age 16. Beta values of all theeparate paths are reported in Figure 1. Boys’ HRt age 11 negatively predicted rule breaking atge 16 (� � �0.07, t � �1.74, p � .04) and wasegatively associated with the EATQ-R surgencyeasure (� � �0.06, t � �1.74, p � .04). Regres-

ion analyses showed that the association be-ween boys’ HR and rule breaking dropped intrength, while allowing surgency at age 11 toediate this relationship (mediation effect: � �0.05, t � �1.16, p � .13). This mediation effectid not reach significance in the Sobel and boot-trapping test. In girls, HR was associated onlyith surgency (� � �0.12, t � �3.42, p � .01).In boys, lower HR was significantly associated

ith more aggression at age 16 (� � �0.09, t �2.32, p � .01); but, again, personality (effortful

ontrol) did not mediate this relationship. Inirls, HR was not associated with effortful con-rol or aggression, and thus no mediation effects

ere found. Boys and girls low on effortfulontrol at age 11 were more aggressive at age 16for both, � � �0.15, t � �3.54, p � .001).

R and ASB: BIS/BASesults of the mediation analysis with the BIS/AS measures are presented in Figure 2. HR wasegatively associated with fun seeking at age3.5 (� � �0.07, t � �1.90, p � .03 for boys,nd � � �0.06, t � �1.77, p � .04 for girls).

its in Study Population: Means, Standard Deviations,

Boys Gender Differences

N Mean SD T df p

51 75.36 10.60 6.49 1751 �.00180 3.11 0.70 7.28 1607 �.00181 3.41 0.91 �4.84 1603 �.001

00 2.37 0.50 11.93 1656 �.00100 2.70 0.50 �1.40 1656 .16

19 0.15 0.18 �6.06 1331 �.00119 0.29 0.17 �5.78 1332 �.00119 2.77 0.52 3.42 1330 �.0119 3.73 0.55 �7.50 1330 �.001

en boys and girls. BAS � Behavioral Activation Scale; BIS � BehavioralTemperament Questionnaire Report–Revised, NEO-PI-R � Neuroticism-rt.

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cantly associated with rule breaking at age 16(� � 0.13, t � 3.11, p � .01). As hypothesized,there was evidence that boys’ fun seeking atage 13.5 mediated the relationship between HRand rule breaking (Figure 2). The Sobel test(Z � �1.66, p � .05) and the bootstrappingmethod (�0.0002; 95% CI between �0.0003 and.0000) showed that the mediation effect wasmarginally significant. Behavioral inhibitionwas unrelated to HR and aggression and thusno mediation effects were found.

HR and ASB: NEO-PI-RHR at age 11 was negatively associated with

FIGURE 1 Graphic presentation of the associations betand antisocial behavior; heart rate and antisocial behavioregression beta values belonging to the particular pathwa.05] are given in boldface type; Boys are represented abmediation effects of personality on the relationship betweassessed at age 11 years via the Early Adolescent Tempebeats per minute. aMediation significant.

adventurism at age 16 (� � �0.16, t � �4.13, p m

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.01 for boys, and � � �0.09, t � �4.13, p �01 for girls). Boys’ adventurism at age 16

ediated the relationship between HR and rulereaking, because the association between HRnd rule breaking came close to zero (� �0.02, t � �0.55, p � .29; Figure 3), while

llowing for mediation of adventurism. Theobel test (Z � �3.61, p � .001) and theootstrapping method (�0.0008; 95% CI be-ween �0.0012 and �0.0004) showed that thiseduction of the direct association between HRnd rule breaking was significant. In girls andoys, impulsivity was associated with aggres-ion (� � 0.31, t � 8.82, p � .001). However, no

the following: heart rate and personality; personalitynd the mediating effect of personality. Note: Values arene-tailed tests; significant regression beta values [p �he line and girls below. Dashed lines indicate indirect orart rate and antisocial behavior). Personality wasnt Questionnaire Report–Revised (EATQ-R). Bpm �

weenr; ays (oove ten herame

ediation effects were found, because HR was

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not associated with impulsivity or aggression(in girls).

DISCUSSIONWe showed that it is useful to distinguish betweenboys and girls and subtypes of ASB when studyingthe relationship between HR and ASB. Moreover,in boys, we were able to show part of the underly-ing mechanism of the relationship between lowresting HR at age 11 and rule breaking at age 16,namely, the mediating role of sensation seeking atage 13.5 and 16. More importantly, in line with our

FIGURE 2 Graphic presentation of the associations betand antisocial behavior; heart rate and antisocial behavioregression beta values belonging to the particular pathwa.05] are given in boldface type. Boys are represented abmediation effects of personality on the relationship betweassessed at age 13.5 via the Behavioral Inhibition Scale/minute. aMediation significant.

age-effect hypothesis, this relation was not medi- s

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ted by behavioral inhibition and thus providesvidence for different associations between HR inreadolescence and ASB in adolescence. In girls, noediation effects were found.The current study has some limitations. First, we

ould not make statements about the predictivealue of HR on ASB. Our findings show only thatR at age 11 is related to ASB at age 16, but not to

hange in ASB from age 11 to 16. Our secondimitation was the assessment of behavioral inhibi-ion. Ideally we wanted to assess a measure ofmpulsivity or a lack of being able to control one’swn behavior. Although our effortful control mea-

the following: heart rate and personality; personalitynd the mediating effect of personality. Note: Values arene-tailed tests; significant regression beta values [p �he line and girls below. Dashed lines indicate indirect orart rate and antisocial behavior). Personality wasvioral Activation Scale (BAS/BIS). Bmp � beats per

weenr; ays (oove ten heBeha

ure (EATQ-R) came close, there were some items

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that were more related to cognitive than behavioralinhibition constructs. The assessment of the BIS/BAS scales was ideally timed, on average 2 yearsafter HR and 3 years before ASB assessment. How-ever, the BAS fun-seeking scale had low internalconsistency. The NEO-PI-R measure of impulsivitywas the most ideal tool to assess behavioral inhibi-tion. To overcome limitations and to increase com-parability with other studies, we included all threemeasures of behavioral inhibition and sensationseeking. In this way we showed robust findingsregarding the mediating roles of personality char-acteristics in adolescence. Third, we only found

FIGURE 3 Graphic presentation of the associations betand antisocial behavior; heart rate and antisocial behavioregression beta values belonging to the particular pathwa.05] are given in boldface type. Boys are represented abmediation effects of personality on the relationship betweassessed at age 16 via the Neuroticism-Extroversion-Opebeats per minute. aMediation significant.

partial mediation of personality; this means that o

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here are other factors that may also mediate theelationship between HR and ASB.

Apart from these limitations, our study haseveral strong points. We were able to study ahysiological measure in relation to psychopathol-gy in a large, nonclinical, general population.oreover, we assessed both parent- and self-re-

orted personality characteristics at different timeoints and showed robust findings with regard to

he relation with HR and ASB. Using differentaters at different ages had advantages. In preado-escence, children were on average 11 years old,nd parents may thus have had a better perspective

the following: heart rate and personality; personalitynd the mediating effect of personality. Note: Values arene-tailed tests; significant regression beta values [p �he line and girls below. Dashed lines indicate indirect orart rate and antisocial behavior). Personality wass Personality Inventory–Revised (NEO-PI-R). Bpm �

weenr; ays (oove ten hennes

n the child’s personality at that time. However, in

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early and middle adolescence, when participantswere on average 13.5 and 16 years old, youth aremore likely to have a clearer perspective on theirown personality than their parents.

As suggested on a theoretical basis,1 we showedthat lower HR was associated with more sensationseeking in adolescent boys, which was in turnassociated with higher levels of rule breaking. Ourfindings were also partly in accordance with previ-ous studies in which the age-specific effects of HRon ASB and of HR on personality were found. Weshowed that boys’ HR was related only to sensationseeking at age 13.5 and 16, and not at age 11.Although we did not find support for the relation-ship between HR and behavioral inhibition in pre-adolescence, this relationship was also absent atages 13.5 and 16, as we predicted. These findingsare partly in line with research that suggests thatafter childhood, behaviorally disinhibited childrenbecome more open to novelty (or sensation) seek-ing later in life.20 Although we did not find amediation effect of behavioral inhibition in pread-olescence, there was an indication that the media-tion effect of sensation seeking became strongerduring adolescence. This effect could at least offersome explanation to the increase of sensation seek-ing and rule breaking in adolescence found previ-ously.19

In the current study, interesting gender differ-ences were found. HR predicted rule breaking andaggression only in boys, and not in girls. Taking acloser look at Ortiz and Raine’s meta-analysis,1 itturns out there were only two studies amongadolescent girls in which associations between HRand ASB were found. These studies had relativelysmall sample sizes (N � 36 and N � 44) and theassessment of ASB in one study is questionable (i.e.,disruptive behavior as rated by teachers). How-ever, there is stronger evidence that fails to repli-cate that low resting HR is associated with ASB inadolescent girls.36-38 In a sample of late adolescents(16 to 18 years; N � 585), only antisocial boys hadlower resting HR.37 Furthermore, in a clinical sam-ple of girls (12.5 years; N � 206), no significantassociation between HR and conduct disorder wasfound.38 Along with the findings in the presentstudy, this may have implications for future studiesassessing the association between HR and adoles-cent girls’ ASB.

In line with a previous study,10 HR was associ-ated with aggression in adolescent boys. Findingsare mixed however, because in a recent study

among adopted adolescents it was shown that low

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esting HR was associated only with rule breakingnd not aggression.9 A possible reason for theseifferent results may be that aggression is a moreeterogeneous construct compared with rulereaking. Whereas the latter is generally related toelinquency, aggression taps into a wide range ofehaviors entailing many different forms (andunctions) related to different outcomes.39,40 Instru-

ental (or proactive) aggression, for instance, isntended behavior and may therefore be unrelatedo behavioral inhibition. This difference in aggres-ion also shows up in the findings that instrumen-al aggression has been associated with low resting

R, whereas reactive aggression, as a direct re-ponse to stimuli, was unrelated to resting HR.41

herefore, future studies may profit from distin-uishing between different types of aggressive be-avior and assessing HR both during rest andental stress conditions to obtain HR reactivityeasures.Based on the fearlessness theory, we expected, in

readolescence, that low behavioral inhibitionould mediate the negative relationship betweenR and aggression. However, we did not find thisediation effect and thus we did not find evidence

or the fearlessness theory. This finding may benterpreted in light of findings indicating that ex-ernalizing problems up until early adolescence arelso partly related to anxiety problems.42,43 Thereay thus be important differences in the underly-

ng mechanisms leading to adolescent ASB. On thene hand, we have a group of (especially male)outh who are characterized by high levels of fearnd anxiety. On the other hand, however, we dealith a group that is characterized by low levels of

ear and anxiety as suggested by fearlessness theo-y.44 Future studies are needed to unravel theseossible group differences.

Ortiz and Raine’s1 meta-analysis resulted in anverall average effect size of d � �0.44, indicating

ower resting heart rate in antisocial children com-ared with both normal controls and psychiatricontrols. In the current study, for boys, calculationsf effect sizes from correlations45 showed smallffect sizes (d � �0.19 for the negative relationshipetween HR and aggression and d � �0.14 for theegative relationship between HR and rule break-

ng). These differences in effect sizes in our studyompared with the meta-analysis may be causedy publication bias, which is known to inflate effectstimates that tend to be in the hypothesized direc-ion in meta-analyses.

In sum, boys with lower HR in preadolescence

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HEART RATE AND ANTISOCIAL BEHAVIOR

appeared to be most at risk for rule breaking andaggression at age 16 years. In line with our age-effect hypothesis, sensation seeking mediated therelationship between HR and rule breaking only inadolescence but not in preadolescence. For inter-vention practices, this has several implications. Assuggested by Ortiz and Raine,1 interventions thatteach youths to engage more in prosocial, law-abiding activities could provide other ways tosatisfy sensation seeking in adolescence and thus tomore optimal levels of autonomic arousal. How-ever, one such cognitive behavioral intervention,aimed at reducing oppositional and aggressivebehavior, positively affected only children withrelatively high HR.46 Those with significantly lowerHR did not profit from the intervention. This showsthat it is difficult to provide activities for youth withthe lowest HR that can fulfill the same need ofsensation as, for instance, rule breaking can. Fromanother perspective, given the mediation effect ofsensation seeking, low HR may not only be associ-ated with rule breaking or other ASB but may alsobe associated with risky behavior in general. Tak-ing more risk may have negative consequences(e.g., stealing may lead to incarceration), but canalso have beneficial effects (e.g., stepping up forsomeone in a fight may be socially rewarding),making the behavioral effects associated to low HRdependent upon contextual factors as well.

Finally, we want to address the discussion onwhether resting HR could, and should, be used asa marker of the development of ASB over time.3

Our findings showed that HR measures obtained

with a strict acquisition and analysis protocol were

conductance in behaviorally inhibited Mauritian children. J Ab-norm Psychol 1997;106:182-190.

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VOLUME 49 NUMBER 5 MAY 2010

ssociated with ASB in boys but not in girls. De-pite the small effect sizes, the relative ease ofssessing HR at rest, even when using a protocol,he robust findings (see the meta-analysis by Ortiznd Raine1), and the associations with ASB overime (current study), could make HR a valuableddition to the early identification of behavioralroblems in boys. &

Accepted February 18, 2010.

Mr. Sijtsema, Drs. Veenstra, and Lindenberg are with the University ofGroningen. Dr. Veenstra is also with the University of Turku. Drs. vanRoon, Ormel, and Riese are with the University Medical CenterGroningen. Dr. Verhulst is with the Erasmus University Medical Centre–Sophia Children’s Hospital Rotterdam.

This research is part of the TRacking Adolescents’ Individual LivesSurvey (TRAILS). Participating centers of TRAILS include various depart-ments of the University Medical Center Groningen and University ofGroningen, the Erasmus University Medical Center Rotterdam, theUniversity of Utrecht, the Radboud Medical Center Nijmegen, and theTrimbos Institute, all in the Netherlands. Principal investigators are J.Ormel and F.C. Verhulst. TRAILS has been financially supported byvarious grants from the Netherlands Organization for Scientific Re-search (NWO) (for grant details, see www.trails.nl); the SophiaFoundation for Medical Research (projects 301 and 393); the DutchMinistry of Justice (WODC); and the participating universities.

The authors are grateful to all adolescents, their parents, and teacherswho participated in this research and to everyone who worked on thisproject and made it possible. We thank also Prof. A.J. Oldehinkel andthe scientific meeting group Wednesday Afternoon Lunch Meeting(WALM) for their input.

Disclosure: Dr. Verhulst is a contributing author of the AchenbachSystem of Empirically Based Assessment, from which he receivesremuneration. Drs. Sijtsema, Veenstra, Lindenberg, van Roon, Ormel,and Riese report no biomedical financial interests or potential conflictsof interest.

Correspondence to: Jelle Sijtsema, Department of Sociology,University of Groningen, 9712 TG Groningen, the Netherlands;e-mail: [email protected]

0890-8567/10/©2010 American Academy of Child and Adoles-cent Psychiatry

DOI: 10.1016/j.jaac.2010.02.005

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