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Received: 11 July 2016 | Accepted: 1 April 2017

DOI: 10.1002/dev.21522

BRIEF REPORT

Afternoon cortisol provides a link between self-regulated


anger and peer-reported aggression in typically developing
children in the school context

Eva Oberle PhD1 | Kaitlyn McLachlan PhD2 | Nicole L.A. Catherine PhD3 |
Ursula Brain BA4 | Kimberly A. Schonert-Reichl PhD5 | Joanne Weinberg PhD6 |
Tim F. Oberlander MD, FRCPC4
1 School of Population and Public Health, The
Human Early Learning Partnership, The Abstract
University of British Columbia, Vancouver,
Aggression jeopardizes positive development in children and predicts social and academic
British Columbia, Canada
2 Department
maladjustment in school. The present study determined the relationships among anger
of Psychiatry, University of
Guelph, Guelph, Ontario, Canada dysregulation (a marker of emotion regulation), cortisol activity (a biomarker of stress), and peer-
3 Simon Fraser University, Children’s Health nominated aggression in typically developing children in their everyday classroom setting
Policy Center, Vancouver, British Columbia, (N = 151, Mean age = 10.86, SD =.74). Salivary cortisol was collected at 09:15, 11:45, and
Canada
14:45 hr across 4 consecutive days. Children provided self-reports of anger regulation; peers
4 Department of Pediatrics, The University of reported proactive and reactive aggressive behaviors. Hierarchical linear regression analyses,
British Columbia, Vancouver, British Columbia,
Canada
followed by a bootstrapping analysis identified basal afternoon cortisol as a significant mediator
5 Department of Educational and Counselling
between anger regulation and peer-reported aggression. More dysregulated anger significantly
Psychology, and Special Education, The predicted lower afternoon cortisol, which in turn predicted increased peer-reported aggression.
University of British Columbia, Vancouver, These results align with previous research on links among hypocortisolism, emotional
British Columbia, Canada
regulation, and behavior, and suggest a possible meditational pathway between emotion and
6 BC Children’s Hospital Research Institute,
behavior regulation via decreased afternoon cortisol levels.
Department of Pediatrics, School of Population
and Public Health, The University of British
Columbia, Vancouver, British Columbia, Canada KEYWORDS
Correspondence aggression, cortisol, emotion regulation, peer reports, school-based research
Eva Oberle, School of Population and Public
Health, The University of British Columbia, 2206
East Mall, Vancouver, BC V6T 1Z3, Canada.
Email: eva.oberle@ubc.ca
Funding information
The Human Early Learning Partnership, UBC

1 | INTRODUCTION (Dodge & Coie, 1987; Dodge, 1991; Scarpa, Chiara, & Tanaka, 2010).
Proactive aggression (PA)—known as “cold tempered aggression”—has
Reactive and proactive aggression are two subtypes of aggression that been described as a deliberate behavior that occurs unprovoked and is
have been linked to a range of maladjustment indicators, including typically used to intimidate a person or to achieve some goal (Card
peer rejection, academic failure, and suspension from school (Card, et al., 2006). Despite established distinctions, RA and PA tend to be
Little, Card, & Little, 2006; Hubbard, McAuliffe, Morrow, & Romano, highly correlated and often co-occur in children demonstrating
2010; Miller-Johnson, Coie, Maumary-Gremaud, & Bierman, 2002; aggressive behaviors (Scarpa et al., 2010).
Valois, Macdonald, Bretous, Fischer, & Drane, 2002). Reactive A theoretical and empirical link has been established between lower
aggression (RA)—known as “hot tempered aggression”—is an angry levels of self-regulation and higher levels of RA (de Castro, Merk, Koops,
response to perceived provocation; it is associated with difficulty Veerman, & Bosch, 2005; Eisenberg, Spinrad, & Eggum, 2010; Frick &
encoding social cues and responding aggressively to social conflict Morris, 2004; Lopez-Duran, Olson, Hajal, Felt, & Vazquez, 2009). While

Developmental Psychobiology. 2017;9999:1–8. wileyonlinelibrary.com/journal/dev © 2017 Wiley Periodicals, Inc. | 1


2 | OBERLE ET AL.

anger has been considered a driving force of RA (Hubbard, McAuliffe, axis activity also underlies the link between emotion regulation and
et al., 2010), the research on emotion-regulation in PA has been aggression is still unclear.
equivocal. Most researchers have argued that children who tend to be The HPA axis is a central part of the neurobiological stress
proactively aggressive do not consistently exhibit problems with self- response system. This system involves a cascade of hormones from
regulatory processes (Lopez-Duran et al., 2009), while some empirical the hypothalamus to the pituitary to the adrenal gland, resulting in the
research has found a link between lower levels of emotion-regulation release of the stress hormone cortisol from the adrenal cortex (Jessop
ability and higher levels of PA (de Castro et al., 2005; Xu, Farver, & & Turner-Cobb, 2008). Optimacl activity and regulation of the HPA
Zhang, 2009). axis is critically important to health (Gunnar & Quevedo, 2007). In the
The goal of the present study was to investigate the role of typical HPA diurnal pattern, cortisol levels are high at awakening, rise
emotion-regulation (i.e., anger regulation) and underlying physiological further within 20–45 min after waking (the cortisol awakening
processes (i.e., daily cortisol activity) in aggression in typically response, CAR), and then gradually decline across the day,
developing children. Given theoretical considerations (Eisenberg with lowest concentrations in the evening. Inappropriately elevated
et al., 2010) and previous research findings on the link between anger or low cortisol levels and failure to downregulate cortisol throughout
regulation and RA (Hubbard, McAuliffe, et al., 2010), the main the day may indicate compromised HPA axis functioning and thus
aggression outcome of interest in the present study is RA. Because altered physiological regulation (Gunnar & Vazques, 2001; Jessop &
RA and PA overlap considerably and may co-occur in children (Scarpa Turner-Cobb, 2008; Miller, Chen, & Zhou, 2007).
et al., 2010), we also include PA as a secondary focus. Investigating Research that has linked basal cortisol and externalizing behaviors
underlying physiological processes involved in anger regulation and has found mixed results. A number of previous studies have consistently
both forms of aggression is also of interest because it allows exploration found lower basal cortisol concentrations in children and adolescents
of whether predictive patterns for RA and PA differ or overlap. who persistently display aggressive and antisocial behaviors (Alink et al.,
This study offers a novel contribution to the extant literature. We 2008; Gunnar & Vazques, 2001; McBurnett, Lahey, Rathouz, & Loeber,
focus on typically developing children in their everyday classroom 2000; Shirtcliff & Essex, 2008; Susman, 2006; van Goozen, Fairchild,
instead of a clinical sample representing only a small portion of the Snoek, & Harold, 2007). However, some studies have also found the
population (i.e., the 12-months prevalence rate for clinical conduct opposite pattern, with higher basal cortisol levels linked to more
disorder was 2.1% in a recent study with 8–15-year-old children; externalizing behaviors (Hart, Burock, London, Atkins, & Bonilla-
Merikangas et al., 2010). Aggression occurs in typically developing Santiago, 2005; van Bokhoven et al., 2005). In their meta-analytic
children on a regular basis (Catherine, Schonert-Reichl, Hertzman, & review, Alink et al. (2008) found that age moderated the relationship
Oberlander, 2012) and is a frequent reason for adjustment challenges in between cortisol and externalizing behaviors. In fact, whereas lower
and outside school (Hubbard, Smithmyer, et al., 2010; McAdams & basal cortisol was significantly related to higher levels of aggression in
Lambie, 2003). It is thus important to conceptualize aggressive behaviors school-aged children, the correlation between cortisol and aggression in
as a continuous dimension that exists to varying degrees in each child, early childhood (i.e., before age 5) was a significantly positive one. As a
and investigate the involved emotional and physiological processes. possible explanation, the authors discussed a bidirectional process
Research on the physiological processes (e.g., cortisol activity) between HPA functioning and problem behavior. Specifically, during
involved in aggression is still at an emergent stage (Alink et al., 2008; early childhood, children with higher levels of externalizing behaviors
Catherine et al., 2012). Such research is critical because it can reveal might be subject to harsher punishment by parents. This, in turn, may
processes underlying social behaviors and identify potential physiological contribute to higher levels of stress in young children, which could affect
markers of aggression (Susman, 2006). In addition to a strong focus on HPA functioning, and contribute to higher basal cortisol levels. If stress
clinical samples and studies conducted in laboratory settings, a further continues over an extended time period (i.e., allostatic load), down-
limitation of previous research on physiological processes underlying regulation of the HPA axis may occur by the time children reach middle
aggression is the reliance on teacher reports of children’s externalizing childhood, which would be reflected in lower concentrations of cortisol.
behaviors (Card et al., 2006). Teachers’ observations are often restricted Two further explanations have been offered for the finding that
to classroom interactions and many aggressive behaviors may occur when children with lower basal cortisol levels exhibit higher levels of
they are unaware. Hence, in the present study we drew from collective aggression. The stimulation-seeking theory suggests that children with
reports of classroom peers about each child’s externalizing behaviors in low basal cortisol seek stimulation to increase their arousal levels to a
the school context in determining RA and PA. more optimal state (van Goozen et al., 2007). This might be reflected in
the inverse association between low basal cortisol and externalizing
behavior problems (Alink et al., 2008; Susman, 2006). Alternatively,
1.1 | Neurobiological mechanisms involved in PA
the fearlessness theory suggests that low cortisol concentrations
and RA
reflect fearlessness and a lack of inhibition underlying aggressive
Failure to regulate strong negative emotions such as anger has been behaviors (Raine, 2002).
linked to aggression in children (Eisenberg et al., 2010). The activity of Against this background, researchers have consistently linked poor
the hypothalamic–pituitary–adrenal (HPA) or stress axis is known to emotion regulation to aggressive behaviors in children. Specifically, the
be involved in both the regulation of emotions (Stansbury & Gunnar, link between anger regulation and RA has been widely supported
1994) and in childhood aggression (Alink et al., 2008). Whether HPA (Eisenberg et al., 2010; Hubbard, Smithmyer, et al., 2010). Previous
OBERLE ET AL.
| 3

research has also indicated the role of cortisol in externalizing behaviors a large public school district in Western Canada. Schools were in urban
(e.g., Alink et al., 2008). However, to this point, it is unclear whether middle class neighborhoods (Median neighborhood family income:
cortisol may also play a role in the relationship between anger regulation CA$74,491 and CA$76,691). Participation rates in the two schools
and aggression. Exploring this question is critical. It can provide insights were 94% and 86%. Most children reported English (52%) as their first
into the underlying pathways involved in aggressive behaviors in language, followed by Cantonese or Mandarin (29%), and other languages
typically developing children. Conducting this research in children’s day- (e.g., Tagalog) representative in the neighborhood. All participating
to-day environment—the school—is a strength of this study as the children were competent in reading and writing English. Two thirds (67%)
findings have practical relevance and help researchers and educators lived with both parents, one quarter (24%) lived with one of their parents,
understand the processes involved in externalizing behaviors in the and the remainder reported alternative family compositions (e.g., foster
general population of school-aged children. care, living with grandparents or relatives). All children had received
parental consent and provided assent.
1.2 | The present study
2.2 | Procedure
The main goal of the present study was to examine relationships
among peer-reported RA, anger dysregulation, and the daily pattern of Self- and peer-report surveys were administered by research assistants
basal cortisol in the classroom context. We predicted that lower basal in the classroom during a regular class period at the end of the school
cortisol and higher anger dysregulation would both be linked to RA year in the spring. Items were read out loud. After survey completion,
(Alink et al., 2008; Eisenberg et al., 2010; Hubbard, Smithmyer, et al., research assistants visited each classroom three times per day over four
2010; Susman, 2006), and that more dysregulated anger—given its link consecutive days (i.e., Tuesday through Friday) to collect saliva samples.
to aggressive behavior—would be significantly related to lower basal On each of the days, saliva was sampled at 09:45, 11:45, and 14:45 hr,
cortisol. The role of basal cortisol as a partial or full mediator between resulting in a total of 12 samples per subject. Samples were transferred
anger dysregulation and RA was further explored. Given that RA and to a laboratory for analysis of cortisol immediately after collection. The
PA have been found to overlap considerably, and yet are described as university and school district ethics boards provided approval.
different phenotypes of aggression, a secondary goal of this study was
to investigate whether the predictive pattern revealed for RA would 2.3 | Measures
differ or replicate for PA.
Means, standard deviations and correlations among all variables are
shown in Table 1.

2 | M E TH O D 2.3.1 | Demographics
Children completed a brief demographic survey.
2.1 | Participants
Participants were 151 typically developing students (43% boys) in 4th to 2.3.2 | Anger regulation
6th grade (Mean age = 10.86 years, SD =.73, Range = 9.37–10.09 years). We administered a three-item Anger subscale of the Children’s Emotion
Data were collected in six elementary school classrooms in two schools in Management Scale: Anger (Zeman, Shipman, & Penza-Clyve, 2001),

TABLE 1 Study variables descriptive information and intercorrelations between all variables
Variable name Mean (SD) 1. 2. 3. 4. 5. 6. 7. 8. 9.
1. Age 10.86 (.74) –
2. Gendera n/a .049 –
3. Anger dysregulationb 1.78 (.35) .090 .053 –
4. 9:15 am cortisol (nmol/L) c
.81 (.22) .169* −.171* −.087 –
5. 11:45am cortisol (nmol/L)c .57 (.18) −.099 .157† −.139† .011 –
6. 2:45pm cortisol (nmol/L) c
.52 (.16) .011 .056 −.208* .181* .566*** –
7. Slope −.05 (.05) −.123 .163† −.055 −.733*** .346*** .519*** –

8. Time since awaking d
1.82 (.44) −.134 .158 −.116 −.509*** .291*** .071 .469*** –
9. Peer nominated RAe .11 (.10) −.135 −.130 .188* −.065 −.183* −.281** −.143 .086 –
10. Peer nominated PA e
.07 (.10) −.146 −.332*** .166* .082 −.220** −.252** −.258** −.044 .701***
a
1 = male, 2 = female.
b
Higher scores indicate a more dysregulated expression of anger.
c
Raw cortisol was log transformed; cortisol values represent the average of the four samples collected on four subsequent days for each time point.
d
Larger numbers indicate more time between wake-up and 9:15 am sampling.
e
RA = reactive aggression, PA = proactive aggression; peer nominations were standardized within classroom to account for variation in classroom size.

p < .10; *p < .05; **p < .01; ***p < .001.
4 | OBERLE ET AL.

assessing children’s dysregulation of anger expression. On a three-point study. For each question, they were asked to circle the names of as many
scale, children indicate 1 (hardly ever true), 2 (sometimes true), or 3 (often or as few of their classmates who fit each behavioral description. The
true) for the statements “I do things like slamming the door when I am percentage of nominations each student received for each item was
mad,” “I attack whatever it is that makes me mad,” and “I say mean things computed by dividing the number of nominations received by the total
to others when I am mad.” Higher mean scores indicated more number of participating students in the classroom. Peer nominations of
dysregulated expression of anger. The internal consistency of the scale aggressive behaviors represent aggregated perceptions of all classmates,
was adequate (Cronbach’s α =.60) and comparable to previous studies standardized according to classroom size, and have been found reliable
(Mclaughlin, Hatzenbuehler, & Hilt, 2009; Sim & Zeman, 2005). and valid in previous research (Catherine et al., 2012; Crick & Dodge,
1996).
2.3.3 | Salivary cortisol
Materials for collecting saliva samples were obtained from Salimetrics,
LLC, State College, PA. Saliva samples were collected using a sterile
3 | RE SULTS
cotton swab held in the mouth, between teeth and cheek, for
approximately 2 min. The swab was then placed inside an internal
container within a plastic tube. In collaboration with the classroom
3.1 | Preliminary analyses
teachers, we restricted high physical activity and food/drink intake Cortisol concentrations at each time point (i.e., 09:15, 11:45, and
before each cortisol collection. Children recorded what time they 14:45 hr) were log transformed and averaged across the four days.
woke up that day, and recorded medication intake (type and time) each Single missing cortisol values (<6%) were replaced by the daily average
morning and afternoon. of that time point for that particular child. After transformation,
Salivettes were centrifuged at 3,000 rpm for 5 min and cortisol cortisol data were normally distributed at each time point of collection.
levels were measured using a commercial immunoassay with Figure 1a illustrates that children’s cortisol levels in an everyday
chemiluminescence detection (CLIA; IBL-Hamburg, Hamburg, classroom setting followed the expected diurnal rhythm: higher
Germany). The lower limit of detection was 0.44 nmol/liter; intra- morning cortisol levels followed by a significant decline by noon and
and inter-assay coefficients of variation were less than 8%. Any sample late afternoon. Separate cortisol slopes were calculated for each of the
over 50 nmol/liter was rerun. four sampling days, regressing the cortisol value at each time point on
awakening time. An average slope composite was created across all
2.3.4 | Peer nominations of aggression days. Data analyses were performed using SPSS 18.0.
Following established procedures (Oberle, Schonert-Reichl, & Thomson, Few children reported medication intake (Mean = 4.3%,
2010; Parkhurst & Asher, 1992), peer nominations were used to obtain SD = 1.76, across all four mornings; Mean = 1.9%, SD = .41, across
independent assessments of RA (i.e., “gets angry easily and fights back all four afternoons). Types of medication reported were asthma puffer,
when teased,” and “gets mad at kids who hurt them by accident”; α =.88) allergy medication, cough medicine, and ADHD medication. Because
and PA (i.e., “plays mean tricks or plans to hurt others,” and “gets other the use of such medications may impact cortisol levels (Granger, Hibel,
students to gang up on a classmate”; α =.92) (Dodge & Coie, 1987). Fortunato, & Kapelewski, 2009), independent sample t-tests were
Students were given a list of all classmates who were participating in the conducted for each of the morning and afternoon cortisol collections

F I G UR E 1 (a) Shows the cortisol regulation from morning to afternoon, averaged across the four sampling days, for children rated as high/
low on PA/RA by peers (median split); (b and c) show afternoon cortisol mediating the link between anger dysregulation and aggressive
behaviors
OBERLE ET AL.
| 5

and daily slopes. Results indicated that cortisol did not differ significant negative predictor in the model; lower cortisol levels predicted
significantly between children who had reported medication intake higher levels of RA (β = −.245, p = .004). When afternoon cortisol levels
and those who had not. were added to the model, the effect of anger dysregulation was no longer
Table 1 shows that only afternoon cortisol was significantly and significant. This finding provided the rationale for testing whether cortisol
negatively related to anger regulation. More dysregulated anger is a statistical mediator between anger dysregulation and RA (Preacher &
predicted lower afternoon cortisol. Afternoon cortisol was also Leonardelli, 2015).
significantly and negatively related to PA and RA. Children with lower
Mediation analysis
basal cortisol levels were rated as significantly more aggressive by their
The bootstrapping procedure PROCESS for SPSS (Hayes, 2013) was
peers. Morning cortisol levels were statistically unrelated to anger
used to test for mediation. The bootstrapping analysis tested the null
dysregulation and indicators of aggression. Slope was significantly and
hypothesis that the indirect path from anger dysregulation to RA
negatively related to PA, with a steeper slope predicting higher levels
through afternoon cortisol was not significantly different from zero
of PA. Slope was unrelated to anger regulation. These preliminary
(see Figure 1b). The 95% confidence interval values ranged from
associations are consistent with theoretically expected relationships
.004 to .033. Given that the confidence interval did not cross zero,
and were explored further in a series of regression analyses.
the null hypothesis was disconfirmed and a mediation model with
afternoon cortisol as the statistical mediator was supported. More
3.2 | Hierarchical linear regression analyses dysregulated anger significantly predicted lower afternoon cortisol
Hierarchical regression analyses were conducted, predicting both RA (β = −.210, p = .013); lower afternoon cortisol significantly predicted
and PA from anger dysregulation and afternoon cortisol. We higher RA (β = −.274, p = .001); the initial significant relationship
controlled for gender and age in all analyses (Jessop & Turner-Cobb, between anger dysregulation and more RA became nonsignificant
2008). Control variables were entered in the first step, afternoon after controlling for the indirect effect of afternoon cortisol
cortisol levels were entered in the second step, and anger (z = 2.047, p =.04).
dysregulation was entered in the third step of the regression (see
Table 2). 3.2.2 | Predicting peer nominated PA
In Block 1, gender significantly predicted PA, with boys exhibiting higher
3.2.1 | Predicting peer nominated RA scores than girls (β = −.313, p < .001). Younger age marginally predicted
None of the control variables significantly predicted peer nominated RA in higher PA (β = −.136, p = .093). Model 1 was overall statistically
Model 1. In Model 2, adding anger dysregulation resulted in a significant significant [adjusted R2 = .104, F (2, 137) = 9.099, p < .001]. Adding
model for explaining RA [adjusted R2 = .048, F (3, 136) = 3.334, p = .021]. anger dysregulation significantly increased the explained variance in the
Anger dysregulation was a significant predictor; more dysregulated model to 13.4% [R2Δ = .036, FΔ (1, 136) = 5.761, p = .018]. More
anger predicted higher levels of RA (β = .189, p =.024). The change of dysregulated anger significantly predicted higher levels of PA (β = .190,
variance explained from Models 1–2 was significant [R2Δ = .036, p = .018). In Block 3, entering afternoon cortisol to the model
FΔ (1, 136) = 5.205, p = .024]. In Block 3, entering afternoon cortisol to significantly increased the variance explained in PA to 16.9%
the model significantly added variance explained in the model [R2Δ = .057, [R2Δ = .040, FΔ (1, 135) = 6.698, p = .011]. Lower afternoon cortisol
Fchange(1, 135) = 8.827, p = .004]. The total variance explained was 10% levels significantly predicted higher levels of PA (β = −.205, p = .011).
[adjusted R2 = .100, F (4, 135) = 4.851, p = .001]. Afternoon cortisol was a After adding afternoon cortisol to the model, the effect of anger

TABLE 2 Results for hierarchical regressions predicting peer nominated reactive and proactive aggression
Reactive aggression Proactive aggression

Variables B SE beta t p B SE beta t p


Block 1
Student age −.018 .012 −.130 −1.553 >.100 −.018 .011 −.136 −1.690 .093
Gender −.026 .017 −.124 −1.478 >.100 −.062 .016 −.313 −3.895 <.001
Block 2
Student age −.020 .012 −.142 −1.717 .088 −.020 .011 −.148 −1.868 .064
Gender −.026 .017 −.127 −1.532 >.100 −.063 .016 −.315 −3.995 <.001
Anger dysregulation .055 .024 .189 2.281 .024 .054 .022 .190 2.400 .018
Block 3
Student age −.020 .011 −.140 −1.731 .086 −.020 .011 −.145 −1.876 .063
Gender −.023 .017 −.114 −1.414 >.100 −.061 .015 −.305 −3.934 <.001
Anger dysregulation .040 .024 .137 1.658 .100 .041 .022 .146 1.841 .068
2:45 pm cortisol −.152 .051 −.245 −2.971 .004 −.123 .047 −.205 −2.588 .011
6 | OBERLE ET AL.

dysregulation dropped to marginal significance (β = .146, p = .068), behaviors, such as early childhood experiences and adversity
providing the rationale for a mediation analysis. (Gunnar & Quevedo, 2007).
Similar relationships for both RA and PA were demonstrated in
Mediation analysis
the current study. Dysregulated anger was associated with higher
Bootstrapping analysis (Hayes, 2013) confirmed a significant media-
levels of PA, with lower afternoon cortisol levels significantly
tion model (see Figure 1c). The 95% confidence interval ranged from
mediating this relationship. Although anger and self-regulation
.003 to .029. Similar to the model for RA, more dysregulated anger
have not been considered a driving factor for PA (Eisenberg et al.,
significantly predicted lower afternoon cortisol (β = −.210, p = .013);
2010; Hubbard, Smithmyer, et al., 2010), some research has
lower afternoon cortisol significantly predicted higher PA (β = −.236,
suggested a link between self-regulation and PA (Xu et al., 2009).
p = .003); the initial significant relationship between anger dysregu-
As suggested in previous theory and research (Eisenberg et al.,
lation and PA was marginally significant after controlling for the
2010), self-regulatory processes might be involved in both PA and
indirect effect of afternoon cortisol.
RA, with different types of self-regulation (i.e., emotional vs.
behavioral) underpinning the two different types of aggression.
The expression of anger regulation measure used in the present
4 | DISCUSSION study taps into both emotional and behavioral aspects of self-
regulation (Zeman et al., 2001). In addition, overlap between PA
The current study examined the pathway from anger dysregulation and RA has been established, suggesting that some of the
and cortisol regulation to both PA and RA in children in everyday underlying processes of PA and RA would also be similar (Dodge
classroom settings. Higher levels of anger dysregulation were linked to & Coie, 1987; Scarpa et al., 2010).
lower afternoon basal cortisol levels, which in turn was linked to higher A possible limitation in the present study was that anger
levels of aggression in elementary school aged children. Specifically, dysregulation was measured with a three-items measure. A longer
afternoon cortisol levels statistically mediated the link between anger and more comprehensive measure could be used in future research
dysregulation and aggressive behaviors. to understand different components of anger regulation and their
Several explanations for our findings are possible. First, link to RA and PA, as well as the underlying physiological
children with high levels of dysregulated anger might also exhibit processes. Future research can also advance the present findings
so-called fearlessness and lack of inhibition; it has been argued by investigating additional predictor variables and exploring to
that fearlessness and a lack of inhibition are reflected in low what degree physiological and self-regulatory processes involved
cortisol and drive aggressive behaviors (Raine, 2002). Second, in PA and RA are shared or differ. Longitudinal research could also
dysregulated anger may stem from children’s under-arousal—a advance the present study by investigating whether aggression
predictor of both lower basal cortisol and higher RA (Alink et al., precedes cortisol or vice versa. Given that the study was
2008; Susman, 2006; van Goozen et al., 2007). Last, dysregulated conducted with typically developing children in a real-life context,
anger in children might lead to social rejection by peers which has the present findings have practical relevance in that they can
been linked to blunted cortisol levels and more behavioral inform educational practices and interventions in the classroom
problems in children (Ouellet-Morin et al., 2011). Further research setting (e.g., programs that target the improvement of self-
is needed to investigate these potential additional mediating regulatory skills in order to prevent or decrease aggression)
pathways and explore the possibility of a directional relationship (Wyman et al., 2010).
from anger dysregulation to cortisol activity to aggression in
longitudinal and experimental designs.
We can only speculate about the role of developmental
5 | C ONC LU SI ON S
pathways in these findings. Possibly, low basal cortisol levels reflect
a “counter-regulatory” response due to long-term exposure to
We identified lower basal cortisol in the afternoon as a mediator
excessive cortisol levels (Miller et al., 2007). Predisposition to
between emotion regulation and aggressive behaviors in typically
aggressive behavior may act as a stressor, initially elevating cortisol
developing children in their day-to-day school environment. This
during early development, then subsequently resulting in external-
finding significantly extends the young field of research on bio-
izing behaviors, which in turn increasingly expose a child to ongoing
behavioral processes underlying aggression, and informs future
stressful experiences, which may downregulate or blunt HPA
research, suggesting a possible meditational pathway between
functioning (McBurnett et al., 2000; Rudolph et al., 2000; Shirtcliff
emotion and behavior regulation via decreased basal afternoon
& Essex, 2008; Susman, 2006). This pattern is also reflected in
cortisol levels.
findings showing that higher cortisol levels have been reported in
very young children with externalizing behaviors but not older
REFERENCES
children (Alink et al., 2008; Bakermans-Kranenburg, Van Ijzendoorn,
Alink, L. R. A., van Ijzendoorn, M. H., Bakermans-Kranenburg, M. J.,
Mesman, Alink, & Juffer, 2008; Kestler & Lewis, 2009). Future
Mesman, J., Juffer, F., & Koot, H. M. (2008). Cortisol and externalizing
research needs to take into account environmental variables outside behavior in children and adolescents: Mixed meta-analytic evidence for
of the classroom that shape cortisol regulation and aggressive the inverse relation of basal cortisol and cortisol reactivity with
OBERLE ET AL.
| 7

externalizing behavior. Developmental Psychobiology, 50, 427–450. self-report measures of children’s anger: Relations to reactive versus
https://doi.org/10.1002/dev.20300. proactive aggression. Child Development, 73(4), 1101–1118.
Bakermans-Kranenburg, M. J., Van Ijzendoorn, M. H., Mesman, J., Alink, Jessop, D. S., & Turner-Cobb, J. M. (2008). Measurement and meaning of
L. R. A., & Juffer, F. (2008). Effects of an attachment-based intervention salivary cortisol: A focus on health and disease in children. Stress, 11(1),
on daily cortisol moderated by dopamine receptor D4: a randomized 1–14. https://doi.org/10.1080/10253890701365527.
control trial on 1- to 3-year-olds screened for externalizing behavior. Kestler, L. P., & Lewis, M. (2009). Cortisol response to inoculation in
Development and Psychopathology, 20(3), 805–820. https://doi.org/ 4-year-old children. Psychoneuroendocrinology, 34(5), 743–751.
10.1017/S0954579408000382.
Lopez-Duran, N. L., Olson, S. L., Hajal, N. J., Felt, B. T., & Vazquez, D. M.
Card, N. A., Little, T. D., Card, N. A., & Little, T. D. (2006). Proactive (2009). Hypothalamic pituitary adrenal axis functioning in reactive and
and reactive aggression in childhood and adolescence: A meta-analysis proactive aggression in children. Journal of Abnormal Child Psychology,
of differential relations with psychosocial adjustment. International 37(2), 169–182. https://doi.org/10.1007/s10802-008-9263-3.
Journal of Behavioral Development, 30(5), 466–480. https://doi.org/
McAdams, C. R. I., & Lambie, G. W. (2003). A changing profile of aggression
10.1177/0165025406071904.
in schools: Its impact and implications for school personnel. Preventing
Catherine, N. L. A., Schonert-Reichl, K. A., Hertzman, C., & Oberlander, School Failure: Alternative Education for Children and Youth, 47(3),
T. F. (2012). Afternoon cortisol in elementary school classrooms: 122–130. https://doi.org/10.1080/10459880309604440.
Associations with peer and teacher support and child behavior. School
McBurnett, K., Lahey, B. B., Rathouz, P. J., & Loeber, R. (2000). Low salivary
Mental Health, 4, 181–192. https://doi.org/10.1007/s12310-012-
cortisol and persistent aggression in boys referred for disruptive
9076-y.
behavior. Archives of General Psychiatry, 57(1), 38–43.
Crick, N. R., & Dodge, K. A. (1996). Social information-processing
Mclaughlin, K. A., Hatzenbuehler, M. L., & Hilt, L. M. (2009). Emotional
mechanisms in reactive and proactive aggression. Child Development,
dysregulation as a mechanism linking peer victimization to inyternal-
67(3), 993–1002. https://doi.org/10.1111/j. 1467-8624. 1996.tb0
ization symptoms in adolescents. Journal of Consulting and Clinical
1778.x.
Psychology, 77(5), 894–904. https://doi.org/10.1037/a0015760.
de Castro, B. O., Merk, W., Koops, W., Veerman, J. W., & Bosch, J. D. (2005). Emotion.
Emotions in social information processing and their relations with
Merikangas, K. R., He, J.-P., Brody, D., Fisher, P. W., Bourdon, K., & Koretz,
reactive and proactive aggression in referred aggressive boys. Clinical
D. S. (2010). Prevalence and treatment of mental disorders among US
Child and Adolescent Psychology, 34, 105–116.
children in the 2001–2004 NHANES. Pediatrics, 125(1), 75–81. https://
Dodge, K. A., (1991). The structure and function of reactive and proactive doi.org/10.1542/peds.2008-2598.
aggression. In D. J. Pepler, & K. H. Rubin (Eds.), The development and
Miller-Johnson, S., Coie, J. D., Maumary-Gremaud, A., & Bierman, K. (2002).
treatment of childhood aggression. (pp. 201–208). Hillsdale, NJ:
Peer rejection and aggression and early starter models of conduct
Lawrence Erlbaum Associates, Inc.
disorder. Journal of Abnormal Child Psychology, 30(3), 217–230.
Dodge, K. A., & Coie, J. D. (1987). Social-information-processing factors in Available online at: http://www.pubmedcentral.nih.gov/articlerender.
reactive and proactive aggression in children’s peer groups. Journal of fcgi?artid=2774087&tool=pmcentrez&rendertype=abstract.
Personality and Social Psychology, 53, 1146–1158.
Miller, G. E., Chen, E., & Zhou, E. S. (2007). If it goes up, must it come down?
Eisenberg, N., Spinrad, T. L., & Eggum, N. D. (2010). Emotion-related self- Chronic stress and the hypothalamic-pituitary-adrenocortical axis in
regulated and its relation to children’s maladjustment. Annual Review of humans. Psychological Bulletin, 133(1), 25–45. https://doi.org/
Clinical Psychology, 6, 495–525. https://doi.org/10.1146/annurev. 10.1037/ 0033-2909. 133.1.25.
clinpsy.121208.131208.
Oberle, E., Schonert-Reichl, K. A., & Thomson, K. C. (2010). Understanding
Frick, P. J., & Morris, A. S. (2004). Temperament and developmental the link between social and emotional well-being and peer relations in
pathways to conduct disorders. Journal of Clinical Child and Adolescent early adolescence: Gender-specific predictors of peer acceptance.
Psychology, 33, 54–68. Journal of Youth and Adolescence, 39(11), 1330–1342.
Granger, D. A., Hibel, L. C., Fortunato, C. K., & Kapelewski, C. H. (2009). Ouellet-Morin, I., Odgers, C. L., Danese, A., Bowes, L., Shakoor, S.,
Medication effects on salivary cortisol: Tactics and strategy to minimize Papadopoulos, A. S., . . . Arseneault, L. (2011). Blunted
impact in behavioral and developmental science. Psychoneuroendocri- cortisol responses to stress signal social and behavioral problems
nology, 34(10), 1437–1448. among maltreated/bullied 12-year-old children. Biological Psychiatry,
Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and 70(11), 1016–1023. https://doi.org/https://doi.org/10.1016/j.biopsy
development. Annual Review of Psychology, 58, 145–173. https://doi. ch.2011.06.017.
org/10.1146/annurev.psych.58.110405.085605. Parkhurst, J. T., & Asher, S. R. (1992). Peer rejection in middle school:
Gunnar, M. R., & Vazques, D. M. (2001). Low cortisol and a flattening of Subgroup differences in behavior, loneliness, and interpersonal
expected daytime rhythm: Potential indices of risk in human develop- concerns. Developmental Psychology, 28(2), 231–241.
ment. Development and Psychopathology, 13, 515–538. Preacher, K. J., & Leonardelli, G. J. (2015). Calculation for the Sobel test: An
Hart, D., Burock, D., London, B., Atkins, R., & Bonilla-Santiago, G. (2005). interactive calculation tool for Mediation tests. Available online at:
The relation of personality types to physiological, behavioural, and http://quantpsy.org/sobel/sobel.htm (Accessed on February 20,
cognitive processes. European Journal of Personality, 19(5), 391–407. 2015).
https://doi.org/10.1002/per.547. Raine, A. (2002). Biosocial studies of antisocial and violent behavior in
Hayes, A. F. (2013). An introduction to mediation, moderation, and conditional children and adults: A review. Journal of Abnormal Child Psychology,
process analysis. New York: The Guilford Press. 30(4), 311–326. https://doi.org/10.1023/A: 1015754122318.
Hubbard, J. A., McAuliffe, M. D., Morrow, M. T., & Romano, L. J. (2010). Rudolph, K. D., Hammen, C., Burge, D., Lindberg, N., Herzberger, D., &
Reactive and proactive aggression in childhood and adolescence: Daley, S. E. (2000). Toward an interpersonal life-stress model of
Precursors, outcomes, processes, experiences, and measurement. depression: The developmental context of stress generation. Develop-
Journal of Personality, 78(1), 95–118. ment and Psychopathology, 12(2), 215–234.
Hubbard, J. A., Smithmyer, C. M., Ramsden, S. R., Parker, E. H., Flanagan, K. D., Scarpa, A., Chiara, S., & Tanaka, A. (2010). Being hot-tempered: Autonomic,
Dearing, K. F., . . . Flanagan, K. (2010). Observational, physiological, and emotional, and behavioral distinctions between childhood reactive and
8 | OBERLE ET AL.

proactive aggression. Biological Psychology, 84(3), 108–116. https:// van Goozen, S. H. M., Fairchild, G., Snoek, H., & Harold, G. T. (2007). The
doi.org/10.1016/j.biopsycho.2009.11.006. evidence for a neurobiological model of childhood antisocial behavior.
Shirtcliff, E. A, & Essex, M. J. (2008). Concurrent and longitudinal Psychological Bulletin, 133(1), 149–182. https://doi.org/10.1037/
associations of basal and diurnal cortisol with mental health symptoms 0033-2909. 133.1.149.
in early adolescence. Developmental Psychobiology, 50(7), 690–703. Wyman, P. A., Cross, W., Hendricks Brown, C., Yu, Q., Tu, X., & Eberly, S.
https://doi.org/10.1002/dev.20336.Concurrent. (2010). Intervention to strengthen emotional self-regulation in children
Sim, L., & Zeman, J. (2005). Emotion regulation factors as mediators with emerging mental health problems: Proximal impact on school
between body dissatisfaction and bulimic symptoms in early adolescent behavior. Journal of Abnormal Child Psychology, 38(5), 707–720.
girls. The Journal of Early Adolescence, 25(4), 478–496. Xu, Y., Farver, J. A. M., & Zhang, Z. (2009). Temperament, harsh and
Stansbury, K., & Gunnar, M. R. (1994). Adrenocortical activity and emotion indulgent parenting, and Chinese children’s proactive and reactive
regulation. Monographs of the Society of Research on Child Development, aggression. Child Development, 80(1), 244–258.
59(2), 108–134. Zeman, J., Shipman, K., & Penza-Clyve, S. (2001). Development and initial
Susman, E. J. (2006). Psychobiology of persistent antisocial behavior: validation of the children’s sadness management scale. Journal of
Stress, early vulnerabilities and the attenuation hypothesis. Neurosci- Nonverbal Behavior, 25(3), 187–205. https://doi.org/10.1023/A:
ence and Biobehavioral Reviews, 30, 376–389. https://doi.org/10.1016/ 1010623226626.
j.neubiorev.2005.08.002.
Valois, R. F., Macdonald, J. M., Bretous, L., Fischer, M. A., & Drane, J. W.
(2002). Risk factors and behaviors associated with adolescent How to cite this article: Oberle E, McLachlan KM, Catherine
violence and aggression. American Journal of Health Behavior, 26(6), NL, et al. Afternoon cortisol provides a link between self-
454–464.
regulated anger and peer-reported aggression in typically
van Bokhoven, I., Van Goozen, S. H. M., van Engeland, H., Schaal, B., developing children in the school context. Developmental
Arseneault, L., Séguin, J. R., . . . Tremblay, R. E. (2005). Salivary cortisol
Psychobiology. 2017;9999:1–8. https://doi.org/10.1002/
and aggression in a population-based longitudinal study of adolescent
males. Journal of Neural Transmission, 112(8), 1083–1096. https://doi. dev.21522
org/10.1007/s00702-004-0253-5.

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