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Biological Psychology 141 (2019) 44–51

Contents lists available at ScienceDirect

Biological Psychology
journal homepage: www.elsevier.com/locate/biopsycho

Skin conductance, heart rate and aggressive behavior type T


a,⁎ b c c c
Todd Armstrong , Jessica Wells , Danielle L. Boisvert , Richard Lewis , Eric M. Cooke ,
Matthias Woeckenerc, Nicholas Kavishd
a
School of Criminology and Criminal Justice, University of Nebraska Omaha, 6001 Dodge Street, Omaha NE, 68182, United States
b
Department of Criminal Justice, Boise State University, Boise ID, 83725, United States
c
School of Criminal Justice and Criminology, Sam Houston State University, Huntsville TX, 77341, United States
d
Department of Psychology, Sam Houston State University, Huntsville TX, 77341, United States

A R T I C LE I N FO A B S T R A C T

Keywords: The current study tested the association between physiology and aggressive behavior type in a large sample of
Skin conductance University students (N = 509). Measures of aggression were gathered with the Reactive and Proactive
Heart rate Aggression Questionnaire. Analyses used raw aggressive behavior type scores and residualized measures of
Autonomic nervous system aggressive behavior type, which account for the overlap between reactive and proactive aggression. Measures of
Reactive
physiology included skin conductance and heart rate, both at rest and in response to a minor social stressor.
Proactive
Analyses assessed the association between aggressive behavior type and measures of physiology in the full
Aggression
sample and in sex specific sub-samples. Results indicated that resting skin conductance was positively associated
with proactive aggression in the full sample and among females. Skin conductance in response to stress had a
positive association with reactive aggression both in the full sample and among males. Skin conductance re-
sponsivity was negatively associated with proactive aggression among males. Findings further strengthen pre-
vious work suggesting that the etiologies of reactive and proactive aggression are distinct and may vary across
sex.

1. Introduction distinction between aggressive behavior types (Hubbard et al., 2010;


Raine et al., 2006). Reactive aggressive behaviors are characterized as
Growing evidence indicates that aggressive behaviors can be ‘hot blooded’ and associated with increased physiological arousal to
meaningfully disaggregated into two distinct but correlated types of stress while proactive aggressive behaviors are characterized as ‘cold
aggression: reactive and proactive (Hubbard, McAuliffe, Morrow, & blooded’ and associated with decreased physiological arousal (Raine
Romano, 2010; Kempes, Matthys, De Vries, & Van Engeland, 2005; et al., 2006).
Vitaro & Brendgen, 2005; see also Bushman & Anderson, 2001). Re- Thus far, the results of studies testing the physiological correlates of
active aggressive behaviors are enacted in response to provocation aggressive behavior type are fairly consistent with the proposed dis-
while proactive aggressive behaviors are instrumental and goal-di- tinction between reactive and proactive aggression. Research in this
rected (Crick & Dodge, 1996; Dodge, 1991). Evidence that reactive and area shows increases in heart rate and skin conductance responsivity
proactive aggressive behaviors actually constitute distinct types of ag- are positively associated with reactive aggression (Hubbard et al., 2002;
gression include studies showing reactive and proactive aggression Murray-Close, Holterman, Breslend, & Sullivan, 2017; Pitts, 1997). In
have different social and psychological correlates (Brendgen, Vitaro, contrast, decreased skin conductance and heart rate in response to
Boivin, Dionne, & Pérusse, 2006; Card & Little, 2006; Cima & Raine, stress are associated with proactive aggression (Bobadilla, Wampler, &
2009; Connor, Steingard, Cunningham, Anderson, & Melloni, 2004; Taylor, 2012; Murray-Close & Rellini, 2012). However, some studies in
Fite, Stoppelbein, & Greening, 2009) and work showing that genetic this area do not find the anticipated association between aggressive
factors differ for reactive and proactive aggression (Baker, Raine, Liu, & behavior type and changes in skin conductance or heart rate (Muñoz
Jacobson, 2008). et al., 2008; Scarpa Haden, & Tanaka, 2010). In addition, work re-
Early models of reactive and proactive aggression focused on social porting significant relationships for one association (e.g., skin con-
information processing (see Crick & Dodge, 1994). Recently, however, ductance reponsivity and reactive aggression) also commonly report
differences in physiological arousal have been characterized as a core null findings for the other association (e.g., skin conductance


Corresponding author.
E-mail address: toddarmstrong@unomaha.edu (T. Armstrong).

https://doi.org/10.1016/j.biopsycho.2018.12.012
Received 24 April 2018; Received in revised form 28 November 2018; Accepted 20 December 2018
Available online 22 December 2018
0301-0511/ © 2018 Elsevier B.V. All rights reserved.
T. Armstrong et al. Biological Psychology 141 (2019) 44–51

responsivity and proactive aggression; see Hubbard et al., 2002). internalizing problems (Card & Little, 2006; Connor et al., 2004).
The current work builds on this emergent literature by testing the
association between skin conductance, heart rate, and aggressive be- 1.2. Physiology and reactive and proactive aggression
havior type as captured by the Reactive and Proactive Aggression
Questionnaire (RPQ; Raine et al., 2006). Analyses are based on a Differences in the etiology of reactive and proactive aggression are
comparatively large sample of University students, and consider phy- also indicated by research testing the association between measures of
siological measures taken at rest and in response to stress. The current physiological arousal and aggressive behavior type. Research in this
work also pays direct attention to potential sex differences in the as- area shows that increases in physiological arousal in response to stress
sociation between physiological reactivity and aggressive behavior captured by skin conductance reactivity (SCR) and heart rate reactivity
type. Differences across sex in the association between physiological (HRR) are associated with reactive aggression in community samples
reactivity (see Hubbard et al., 2002), and differences across sex in the (Hubbard et al., 2002; Murray-Close et al., 2017; Pitts, 1997). In con-
association between physiological reactivity and aggressive behavior trast, decreases in SCR and HRR in response to stress are associated
type are present in work in this area (Bobadilla et al., 2012). However, with proactive aggression in community samples (Bobadilla et al.,
to our knowledge only one study has reported results for sex-specific 2012; Murray-Close & Rellini, 2012). Heart rate (HR) and skin con-
sub-samples (see Bobadilla et al., 2012). ductance (SC) are both indicators of autonomic nervous system (ANS)
activity. The ANS along with the hypothalamic pituitary adrenal (HPA)
1.1. Reactive and proactive aggression axis are the two major divisions of the stress system (Chrousos & Gold,
1992; McEwen & Stellar, 1993). The ANS includes the sympathetic
The concept of reactive aggression is rooted in the frustration-ag- nervous system (SNS) and parasympathetic nervous system (PNS;
gression model (Berkowitz, 1962, 1993). Consistent with this model, Gabella, 2001). The PNS is largely responsible for vegetative and re-
reactive aggression is thought to occur in response to “real or perceived storative function, while the SNS is responsible for the mobilization of
provocation, frustration, or threat and is usually accompanied by the energy under stress. Skin conductance is an index of SNS function,
expression of anger” (Vitaro, Brendgen, & Barker, 2006;). Models of while heart rate is influenced by activity in both the PNS and SNS
social information processing place the proximal etiology of reactive (Akselrod et al., 1981; Robinson, Epstein, Beiser, & Braunwald, 1966;
aggressive behaviors in errors of social information processing in- Warner & Cox, 1962). Consistent with their respective functions, the
cluding hostile attributional bias and difficulty encoding cues (Crick & PNS and SNS exert competing influences on heart rate. Increases in SNS
Dodge, 1994, 1996). More recently, models of aggressive behavior type activity are associated with increases in heart rate and increases in PNS
have begun to specify the role of physiological arousal in the etiology of activity are associated with decreases in heart rate (Glick, Braunwald, &
reactive aggressive behaviors. Within these models, increased heart rate Lewis, 1965; Jänig & McLachlan, 2013). Thus, increases in heart rate in
and skin conductance in response to stress are associated with increased response to stress can be effectuated by the withdrawal of PNS activity
risk for reactive aggression (Hubbard et al., 2010; Scarpa & Raine, and the increase of SNS activity. Alternatively, increases in skin con-
1997, 2000; Scarpa, Haden, & Tanaka, 2010). ductance indicate increased SNS activity, and are not influenced by PNS
Proactive aggression is instrumental or goal-directed aggression activity.
influenced by reinforcement contingencies (Dodge, 1991). The theore- Studies considering the relationship between SCR and aggressive
tical underpinnings of the concept of proactive aggression can be found behavior type among community samples of children and young adults
in the social learning model of aggression (Bandura, 1973, 1983). In the have shown increases in SCR are associated with increased reactive
context of the social learning model, increases in risk for proactive aggression (Hubbard et al., 2002; Murray-Close et al., 2017). Other
aggression stem from exposure to environments that reinforce the use work has shown decreases in SCR are associated with proactive ag-
of goal-directed aggressive behaviors leading to increased positive gression among college students (Bobadilla et al., 2012). These asso-
outcome expectations for proactive aggressive behaviors. Con- ciations are consistent with the proposed distinction in the psycho-
temporary discussions of the etiology of proactive aggression have built physiological etiology of reactive and proactive aggression. However, it
on earlier work by specifying traits and patterns of physiological should be recognized that there is considerable variability across re-
arousal associated with increased risk for proactive aggression (Raine sults. For example, studies finding SCR is positively associated with
et al., 2006). Specifically, proactive aggression is associated with heart reactive aggression, did not find a negative association between SCR
rate and skin conductance hypo-arousal and also associated with de- and proactive aggression in community samples (see Hubbard et al.,
creased sensitivity to distress in others as evidenced by psychopathy 2002; Murray-Close et al., 2017). Similarly, work finding a negative
and callous unemotional traits (Scarpa & Raine, 2000; Raine et al., relationship between SCR and proactive aggression, did not find a po-
2006; Scarpa & Raine, 1997). sitive association between SCR and reactive aggression (Bobadilla et al.,
A number of lines of research now support the distinction between 2012). The proposed association between SCR and aggressive behavior
reactive and proactive aggression. In factor analyses of measures of type failed to present in work by Muñoz, Frick, Kimonis, and Aucoin,
aggressive behavior designed to capture reactive and proactive ag- (2008). In analyses based on a sample of incarcerated male youth, the
gression, items corresponding to aggressive behaviors resulting from authors found the SCR scores of a reactive only aggressive behavior
provocation and attendant emotional arousal typically load on a re- group were not different from the combined aggressive behavior group
active aggression factor, while a second proactive aggressive behavior (reactive and proactive aggression) or a group low on both reactive and
factor is often indicated by items corresponding to goal-directed ag- proactive aggression. It is possible that differences between the results
gressive behaviors without emotional arousal (Cima, Raine, Meesters, & of Muñoz et al. (2008) and studies finding an association between SCR
Popma, 2013; Crick & Dodge, 1996; Day, Bream, & Paul, 1992; Fossati and aggressive behavior type may be explained by the samples used by
et al., 2009; Little, Henrich, Jones, & Hawley, 2003; Poulin & Boivin, the respective studies. Studies finding an association between SCR and
2000; Raine et al., 2006). The distinction between reactive and aggressive behavior type have utilized community samples while the
proactive aggression is also supported by work showing that each type null findings in Muñoz et al. (2008) were based on a forensic sample.
of aggressive behavior has unique socio-environmental correlates Research testing the association between HRR and aggressive be-
(Hubbard et al., 2010). For example, proactive aggression is associated havior type provides some support for the suggestion that increases in
with less prior exposure to victimization, but increased prior exposure HRR are associated with increases in reactive aggression (Pitts, 1997)
to family violence and family substance abuse (Card & Little, 2006; and decreases in HRR are associated with proactive aggression
Connor et al., 2004; Raine et al., 2006). In contrast, reactive aggression (Murray-Close & Rellini, 2012). In a community sample of elementary
is associated with increased prior exposure to abuse and increased school students, Pitts (1997) found a reactive aggressive group showed

45
T. Armstrong et al. Biological Psychology 141 (2019) 44–51

increased heart rate reactivity relative to a nonaggressive group and a the final analysis sample (N=454) was approximately two-thirds fe-
combined aggression group. In work focusing on women, Murray-Close male (N = 305) and one third male (N = 149) with a mean age of
and Rellini (2012) found an association between decreased HRR and 20.30 (SD = 2.90). The racial distribution of the analysis sample was
proactive aggression, but only among women who had been sexually .9% Asian, 11.2% African American, 38.8% Caucasian, 39.2% Hispanic
abused. In contrast, Hubbard et al. (2002) found HRR was not directly and 9.3% Other.
related to either proactive or reactive aggression within a sample of
elementary school boys and girls. 2.2. Procedure
While the majority of studies have not explicitly considered sex
differences in the association between physiological responsivity to After arriving at the laboratory participants were familiarized with
stress and aggressive behavior type, there is evidence of variation in the physiological measurement procedure and informed consent was
levels of SCR and HRR across sex and evidence of variation in the as- reaffirmed. Participants were initially seated and physiological mea-
sociation between SCR and aggressive behavior type across sex. surement sensors were attached to the fingertips of the right hand.
Hubbard et al. (2002) found sex differences in physiological re- Physiological heart rate response was measured using plethysmograph-
sponsivity with boys manifesting higher SCR scores than girls and girls based NeuLog infrared LED transmitter/receptor sensor. Skin con-
having increased HRR relative to boys. Bobadilla et al. (2012) found ductance was measured using NeuLog galvanic skin response sensors
SCR had a negative and statistically significant association with and attached with Velcro connectors. Physiological measures captured
proactive aggression among men (r = −.39, p < .01). The association response to a modified Trier Social Stress Test (Kirschbaum, Pirke, &
between SCR and proactive aggression among females was again ne- Hellhammer, 1993), in which respondents prepared and delivered a
gative but lacked statistical significance (r =−.12, p = .35). speech that addressed their biggest faults and weaknesses. Prior to the
introduction of the stressor, baseline measures were taken after a three
1.3. The current study minute rest period. Participants were then told that they had 2 min to
prepare a 2 min speech on their faults and weaknesses and that this
The current study used a sample of University students to further speech would be recorded. The Time 1 measurement period began
explore the relationship between physiological responsivity and ag- 1.5 min into participants’ speech preparation, just after they were in-
gressive behavior type. This study informs prior work by including formed that the speech would begin shortly. Time 2 measures were
measures of both SCR and HRR and by measuring reactive and proac- gathered as the subjects delivered their speech to a camera. The speech
tive aggression with the RPQ, a widely used self-report measure of was stopped after 2 min and post-stressor measures were gathered. All
aggressive behavior type (Raine et al., 2006). The current study also heart rate and skin conductance measures were calculated as a mean of
extends prior work with an explicit focus on sex differences in SCR and measurements taken every 2 s during the collection window (Baseline:
HRR, and with a focus on sex differences in the association between 30 s, Test 1: 30 s, Test 2: 2 min, Post-test: 30 s).
measures of physiological responsivity and aggressive behavior type. Means and standard deviations of physiological measures at each
The current work also considers the association of resting SC (RSC) and measurement period are presented in Table 1. T-tests were used to
resting HR (RHR) with aggressive behavior type. Prior work has found compare physiological measures at time t-1 to time t. For example, the
RHR rate was negatively associated with proactive aggression (Raine, t-value of 12.83 represents change in heart rate from Baseline to Time 1
Fung, Portnoy, Choy, & Spring, 2014), however other work in this area among females. In general, changes in physiological measures indicate
has shown that RSC is positively associated proactive aggression substantial increases in heart rate and skin conductance after the an-
(Scarpa et al., 2010). nouncement of the task (Baseline to Time 1). Relatively modest declines
during the delivery of the speech (Time 1 to Time 2) and substantial
2. Methods declines after the conclusion of the speech (Time 2 to Post-test). Change
in physiological reactivity for males and females are presented in Figs. 1
2.1. Participants and 2.

Internal Review Board approval was obtained prior to the study.


2.3. Measures
Participants were recruited from criminal justice courses at a university
in a large southern state. All participants provided informed consent
2.3.1. Heart rate and skin conductance measures
and received extra credit for study participation. Measurements in-
SCR and HRR were measured with area under the curve with respect
cluded an in-class survey and a laboratory physiological measurement.
Of the 862 subjects who completed the in-class survey, 556 (64.50%)
Table 1
also completed the laboratory measurement protocol. Those who Heart Rate and Skin Conductance at Each Measurement Period by Sex.
completed the laboratory protocol did not significantly differ from
Females
those that did not in terms of age. Study completion did vary by racial
group (χ2 = 7.72, p < .05) wherein African American participants Heart Ratea Skin Conductanceb
were slightly less likely to participate in physiological measurement
while Hispanic participants were more likely. Females were also sig- Mean t Mean t
nificantly more likely than males to complete the laboratory portion of
Baseline 81.53 3.20
the study (χ2 = 14.76, p < .001). Analyses excluded participants with Time 1 88.20 −12.02*** 4.17 −17.81***
incomplete physiological measures (N = 19; 3.2%), incomplete de- Time 2 87.19 1.89 4.49 6.47***
mographic information (N = 28; 5.0%), or incomplete survey measures Post 79.25 12.41*** 4.15 12.87***
of aggression (N = 47; 8.5%). A single participant indicating that they Males
were a transgender female was also excluded. Finally, analyses ex- Baseline 76.61 4.57
cluded those who were more than three standard deviations from the Time 1 82.60 −7.72*** 5.58 −11.39***
Time 2 81.15 1.69 5.89 −4.47***
mean with regard to either aggressive behavior measures (N = 12;
Post 74.80 7.94*** 5.44 10.93***
2.2%) or physiological measures or (N = 13; 2.3%). Those included in
the analysis were not significantly different from those excluded across Note: a: in beats per minute; b: in microsiemens per minute; t-tests compare
age (t = 1.051; df = 506; p > .05), gender (χ2 = 1.36, p > .05), and measurement at time t-1 to time t; † p < .10,* p < .05, ** p < .01, *** p <
ethnicity (χ2 = 10.31, p > .05). With overlap across exclusion criteria, .001.

46
T. Armstrong et al. Biological Psychology 141 (2019) 44–51

Table 2
Means and Standard Deviations of Measures Physiology and Aggressive
Behavior Type.
Full Sample Females Males t
M/(SD) M/(SD) M/(SD)

Physiological Measure
RSC 3.65 3.20 4.57 6.37***
(2.11) (1.85) (2.29)
RHR 79.91 81.53 76.61 −3.93***
(12.72) (12.61) (12.35)
SCR 229.43 227.74 232.87 .24
(202.35) (191.62) (223.36)
HRR 1139.36 1191.64 1032.35 −.89
(1787.35) (1836.85) (1682.41)

Fig. 1. Male and Female Skin Conductance Across Measurements (in micro- Aggressive Behavior Type
siemens per second). PA .77 .65 1.01 2.64**
(1.22) (1.19) (.65)
RA 5.93 6.01 5.77 .49
(3.59) (3.61) (3.56)

Note: SCR = skin conductance reactivity, HRR = heart rate reactivity,


RSC = resting skin conductance in microsiemens per minute, RHR = resting
heart rate in beats per minute, PA = proactive aggression, RA = reactive ag-
gression; † p < .10,* p < .05, ** p < .01, *** p < .001.

aggression were estimated as the sum of scale items (Reactive aggres-


sion Cronbach’s alpha = 0.77; Proactive aggression Cronbach’s
alpha = .83).1
Means for the RPQ aggression measures presented in Table 2 show
reactive aggression occurred far more often than proactive aggression.
There were sex differences in proactive aggression scores, with proac-
tive aggression scores significantly higher among males. There was no
Fig. 2. Male and Female Heart Rate Across Measurements (in beats per difference across sex in reactive aggression scores. Mean aggression
minute). scores and the differences across sex in aggressive behavior scores re-
ported here are similar to those observed in other work (see Tuvblad
to increase (AUCi; Pruessner, Kirschbaum, Meinlschmid, & et al., 2016).
Hellhammer, 2003). The formula for AUCi is:
n−1 n−1 2.4. Data analysis plan
⎛ (m (i + 1) + mi ) ∙ti ⎞ ⎛ ⎞
AUCi = ⎜ ∑ ⎟ − ⎜m1 ∙ ∑ ti⎟
2
⎝ i=1 ⎠ ⎝ i=1 ⎠ Tests of association between physiological measures and aggressive
where ti is the interval of time between measures and mi is the mea- behavior types utilized the original scale scores for both reactive and
surement itself. In addition to responsivity to stress measured with AUCi proactive aggression as well as residualized aggressive behavior scores.
analyses also considered measures of heart rate and skin conductance at Residualized aggressive behavior type scores serve as a ‘pure’ measure
rest. RSC and RHR were quantified with the baseline measures of heart of aggressive behavior type with covariation across aggressive behavior
rate and skin conductance, respectively. types removed from the residual score. Following the work of Raine
Scores for heart rate, skin conductance, and aggressive behavior et al. (2006), the residualized proactive aggressive behavior measure
measures are summarized in Table 2. Full sample means for RSC and was created by regressing reactive aggression on proactive aggression.
RHR are similar to those presented elsewhere (see Scarpa et al., 2010). Standardized residuals (Mean of 0, SD of 1) from the regression were
Means of physiological measures taken at rest show that, compared to saved as the residualized proactive behavior measure. Similarly, the
males, females had significantly lower RSC, and significantly higher residualized reactive behavior measures was created by saving the
RHR. There were no differences in SC and HR in response to stress (SCR standardized residuals from the regression of proactive aggression on
and HRR) between males and females. reactive aggression.
Analyses first considered the association between physiological
measures taken at rest (RSC and RHR) and aggressive behavior type.
2.3.2. The reactive-proactive aggression questionnaire (RPQ; Raine et al.,
Next, analyses considered the association between physiological re-
2006)
sponse to stress (SCR and HRR) and aggressive behavior type.
The RPQ was used to measure reactive and proactive aggression.
Associations between physiological measures and aggressive behavior
The RPQ consists of 11 items that measure reactive aggression and 12
type were tested with partial correlations in the full sample while
items that measure proactive aggression. The two- factor structure of
controlling for age, race, and sex. For partial correlations, race was
the RPQ has been confirmed in samples of children, adolescents and
represented with dummy variables indicating African American and
adults, and across cultures (Cima, Raine, Meesters, & Popma, 2013;
Hispanic. Gender was indicated with a dummy variable indicating fe-
Fossati et al., 2009; Raine et al., 2006; Tuvblad, Dhamija, Berntsen,
male. Partial correlations were re-estimated with the sample restricted
Raine, & Liu, 2016). Work testing the validity of the RPQ has found
to females while controlling for race and age. These correlations were
reactive aggression as measured by the RPQ is associated with anxiety,
impulsivity, and neuroticism, while the RPQ measure of proactive ag-
gression is associated with callousness, fearless dominance, and bul- 1
Response categories for RPQ items ranged from 0 ‘never’ to 2 ‘often’. Thus,
lying (Cima & Raine, 2009; Cima et al., 2013; Fossati et al., 2009; Raine potential reactive aggression scores ranged from 0 to 22 and potential proactive
et al., 2006). In the current work, measures of reactive and proactive aggression scores ranged from 0 to 24.

47
T. Armstrong et al. Biological Psychology 141 (2019) 44–51

Table 3 inference focuses on the relationship between aspects of physiology and


Partial Correlations between Physiological Measures at Rest (RSC and RHR) and residualized aggressive behavior type measures. In the full sample, in-
Aggressive Behavior Type. creases in RSC were associated with higher proactive aggression scores
PA RA PA Residual RA Residual for both the raw and residualized aggressive behavior measures. The
positive association between RSC and proactive aggressive behavior
Full Sample1 measures found in the full sample was also present when the sample
RSC .109* .037 .128** −.054
was restricted to females. With the sample restricted to males, RSC was
(.016) (.409) (.005) (.239)
RHR .074 .070 .035 .036 not associated with proactive aggression. Returning to the full sample,
(.104) (.120) (.448) (.428) RSC was not related to reactive aggression. RSC was also not associated
Females2 with reactive aggression when the sample was restricted to females.
RSC .148** .064 .158** −.011 When the sample was restricted to males the association between RSC
(.007) (.248) (.005) (.844) and residualized reactive aggressive behavior was negative and showed
RHR .131* .086 .057 .051 a trend towards statistical significance. RHR was not related to re-
(.018) (.119) (.309) (.368)
sidualized measures for either proactive or reactive aggression in the
Males2 full sample, or when the sample was restricted to either females or
RSC −.055 −.014 .094 −.143†
males. However, RHR was related to the non-residualized measure of
(.490) (.864) (.243) (.075)
RHR −.025 .003 .004 −.024 proactive aggression among females.
(.757) (.967) (.959) (.765)
3.1.2. SCR, HRR and aggressive behavior type
Note: SCR = skin conductance reactivity, HRR = heart rate reactivity, Partial correlations coefficients for the association between SCR,
RSC = resting skin conductance, RHR = resting heart rate, PA = proactive HRR, and aggressive behavior type are presented in Table 4. In the full
aggression, RA = reactive aggression; † p < .10,* p < .05, ** p < .01, ***
sample, SCR had a positive association with residualized reactive ag-
p < .001. 1Controlling for age, race, and sex. 2Controlling for age and race.
gression scores. The positive association between SCR and residualized
reactive aggression scores in the full sample was not present among
then re-estimated with the sample restricted to males. Due to kurtosis in
females, but was present among males. In addition, SCR had a negative
proactive aggression measure, partial correlations with proactive ag-
and statistically significant association with residualized proactive ag-
gression model also estimated with log transformed proactive ag-
gression scores among males. Thus, the pattern of association between
gressive behavior scores. When the log transformed proactive ag-
SCR and aggressive behavior scores among males provides particularly
gressive behavior measure was used, the direction and statistical
strong evidence for the divergent validity of reactive and proactive
significance of all coefficients were unchanged. Therefore, results for
aggression, with increases in SCR associated with both increased re-
the untransformed proactive aggressive behavior measures are pre-
active aggression and decreased proactive aggression. Among females,
sented.
the associations between SCR and non-residualized aggressive behavior
measures were positive and showed a trend towards statistical sig-
nificance, while the associations between HRR and both the non-re-
3. Results
didualized and residualized measures of reactive aggression were ne-
gative and showed a trend toward statistical significance
3.1. Physiological reactivity and aggressive behavior type
In the full sample, HRR did not have any statistically significant
association with any aggressive behavior measure. Among females,
3.1.1. RSC, RHR and aggressive behavior type
HRR had a negative association with residualized proactive aggression
Partial correlation coefficients for the association between RSC,
scores that showed a trend towards statistical significance. HRR was not
RHR and aggressive behavior type are presented in Table 3. In order to
associated with any aggressive behavior measure among males.
facilitate comparison, Tables 3 and 4 present both raw and residualized
aggressive behavior type scores. However, discussion and theoretical
4. Discussion
Table 4
A growing number of studies have investigated the physiological
Partial Correlations between Physiological Response to Stress (SCR and HRR)
and Aggressive Behavior Type. correlates of reactive and proactive aggressive behavior. Work in this
area has shown increased SCR and HRR are associated with increased
PA RA PA Residual RA Residual
reactive aggression, while decreased SCR and HRR are associated with
Full Sample 1 increased proactive aggression (Bobadilla et al., 2012; Hubbard et al.,
SCR −.019 .058 −.073 .120* 2002; Murray-Close et al., 2017; Murray-Close & Rellini, 2012; Pitts,
(.647) (.210) (.118) (.011) 1997). In an effort to build on earlier studies, the current work in-
HRR −.067 −.069 −.059 −.013 vestigated the relationship between aspects of physiology and ag-
(.148) (.139) (.211) (.789)
gressive behavior type in a comparatively large sample of University
Females2 students. The current work also investigated potential sex differences in
SCR .094† .097† .042 .071
the association between aspects of physiology and aggressive behavior
(.097) (.086) (.467) (.218)
HRR −.109† .061 −.109† .013 type.
(.054) (.280) (.056) (.825) The results of the current work provide additional evidence that
Males2 increased SCR is associated with increased reactive aggression, while
SCR −.180* −.009 −.237** .207* decreased SCR is associated with increased proactive aggression. This
(.027) (.908) (.004) (.012) pattern is most clear with regard to the relationship between SCR and
HRR .001 .071 .022 −.069 residualized aggressive behavior type measures among males, where
(.999) (.378) (.794) (.404)
increases in SCR were associated with decreases in reactive aggression
Note: SCR = skin conductance reactivity, HRR = heart rate reactivity, and decreases in SCR were associated with increases in proactive ag-
RSC = resting skin conductance, RHR = resting heart rate, PA = proactive gression. The association between SCR and residualized aggressive
aggression, RA = reactive aggression; † p < .10, * p < .05, ** p < .01, *** behavior type measures among males fits well with previously de-
p < .001. 1Controlling for age, race, and sex. 2Controlling for age and race. scribed profiles of reactive and proactive aggression which characterize

48
T. Armstrong et al. Biological Psychology 141 (2019) 44–51

reactive aggression as ‘hot blooded’ in response to provocation RSC and proactive aggression among males. Despite this, the positive
(Hubbard et al., 2010; Scarpa & Raine, 1997, 2000; Scarpa et al., 2010). association between RSC and proactive aggression among females in
The positive association between SCR and residualized reactive ag- the current study and among boys in the work of Scarpa et al. (2010) is
gression was also present in analyses based on the full sample, however seemingly inconsistent with the broader association between decreased
the association between SCR and residualized proactive aggression skin conductance and increased antisocial behavior (Ortiz & Raine,
failed to meet the threshold for statistical significance in the full 2004). It is possible, however, that increased RSC is associated with
sample. deficits in skin conductance fear conditioning which have been shown
The results presented in the current work illustrate the importance to be associated with proactive aggression (Gao, Tuvblad, Schell, Baker,
of considering sex differences in the association between aspects of & Raine, 2015). Skin conductance fear conditioning is indexed by the
physiology and aggressive behavior type. As noted above, results show size of the SC response to a conditioned stimulus after a series of con-
decreased SCR was associated with increased proactive aggression dition stimulus/unconditioned stimulus pairings. Increased RSC may
among males, and increased SCR was associated with increased male then be associated with an attenuated SC response when RSC is ele-
reactive aggression. However, SCR was not associated with either ag- vated prior to the presentation the conditioned stimulus. Additional
gressive behavior type among females. While these results clearly evidence of a positive association between RSC and proactive aggres-
warrant replication before strong theoretical inference, they do point to sion may warrant further work exploring the varying effects of RSC,
sex differences in the physiological profiles of aggressive behavior type, SCR and skin conductance fear conditioning on aggressive behavior
with SCR having a relatively robust association with aggressive beha- type.
vior type in the expected direction among males but not females. While there is considerable variability across studies testing the
It is possible that sex differences in the association between SCR and association between aspects of physiology and aggressive behavior
reactive aggressive behavior type may be moderated by aspects of type, there is an emerging consistency among studies relating SCR to
neuroendocrine function. Specifically, the increased testosterone/cor- either self- or teacher-reports of reactive and proactive aggression in
tisol ratio among males may strengthen the association between SCR community samples (Hubbard et al., 2002; Murray-Close et al., 2017).
and proactive aggression. The tesotosterone-cortisol ratio has been The current work along with prior studies in this area find evidence for
identified as a marker of increased risk for social aggression (Terburg, a positive association between SCR and reactive aggression. Earlier
Morgan, & van Honk, 2009). Roughly characterized, this model sug- work presenting null findings regarding the association between SCR
gests that increased testosterone/cortisol ratios are associated with an and reactive aggression have used an incarcerated sample (Muñoz
increased willingness to confront threat. Thus, it seems possible that et al., 2008) and a community sample with laboratory measures of
higher testosterone/cortisol ratio among males may increase the like- aggressive behavior type (Bobadilla et al., 2012).
lihood that sympathetic nervous system arousal as indicated by in- In contrast, the role of RHR and HRR in aggressive behavior type
creased skin conductance in response to stress leads to reactive ag- remains at issue. Null findings for the association between RHR and
gression. While we recognize the potential role of neuroendocrine proactive aggression among males and the positive association between
function in the association between SCR and reactive aggressive be- RHR and proactive aggression among females stand in contrast to a
havior is speculative, future efforts to parse biological influences on work showing decreases in RHR are associated with increases in ag-
aggressive behavior type may nonetheless benefit from a consideration gression (see Portnoy & Farrington, 2015). Differences between the
of aspects of both ANS and neuroendocrine function. current results and the larger body of literature showing an association
Speculation regarding the role of biological factors in the explana- between RHR and aggression may be attributed in part to the mea-
tion of sex differences in the association between SCR and reactive surement of aggression. Studies dichotomizing aggression into reactive
aggression should be tempered with a consideration the measurement and proactive aspects pay particular attention to the content of mea-
of aggressive behavior. Sex-specific aggressive behavior type means surement, while studies using broad measures of aggression may cap-
presented in Table 2 show that proactive aggression was uncommon in ture a wider range of behaviors. The suggestion that partitioning ag-
the full sample and even less common among females. It is possible that gression into proactive and reactive components influences the nature
the RPQ is not well suited to the detection of the expression of proactive of the association between heart rate and aggression gains some support
aggressive behaviors in females and that measures specifically designed in the work of Scarpa et al. (2010), who use the Revised Parent Rating
to capture this expression may yield different results. Therefore, it is Scale for Reactive and Proactive Aggression (Brown, Atkins, Osborne, &
possible that the presence of sex difference in aggressive behavior type Milmanow, 1996) and find RHR was not related to either reactive or
in the results presented here is influenced by the measurement of proactive aggression.
proactive and reactive aggression. Future investigations of sex differ- Inquiry as to the nature of the association between aggressive be-
ences in the association between physiology and aggressive behavior havior type and heart rate may also benefit from a disaggregation of
type may benefit from the use of measures that capture a wider range of heart rate into cardiac measures capturing unique parasympathetic and
proactive aggressive behaviors including measure of relational aggres- sympathetic nervous system influences on cardiac activity. For ex-
sion (see Murray-Close, Ostrov, Nelson, Crick, & Coccaro, 2010). ample, sympathetic influences on cardiac activity may be captured by
In the current work, there was important variation in the association measuring pre-ejection period, while parasympathetic influences may
between aggressive behavior type and changes in physiology with re- be captured by respiratory sinus arrhythmia (Beauchaine, Gatzke-Kopp,
sponse to stress, relative to the association between aggressive behavior & Mead, 2007). The results of studies using measures of cardiac activity
type and measures of physiology taken at rest. Decreases in physiolo- that are uniquely associated with specific aspects of ANS function may
gical response to stress were associated with increased proactive ag- vary from the results of studies using measures that aggregate para-
gression, as indicated by negative correlation between SCR and sympathetic and sympathetic influences on cardiac activity. For ex-
proactive aggression among males. In contrast, resting psychophy- ample, increased respiratory sinus arrhythmia has been associated with
siology as indicated by RSC had a positive association with proactive proactive relational aggression among women both directly (Murray-
aggression among the full sample and among females. The positive Close et al., 2017) and in interaction with sexual abuse (Murray-Close &
association between RSC and proactive aggression parallels the results Rellini, 2012). Relational aggressive behaviors include actions “in-
of Scarpa et al. (2010) who found a positive association between RSC tended to hurt or harm others through damage to interpersonal re-
and parent reports of proactive aggression in a community sample of lationships” (Murray-Close et al., 2017, p. 79). Thus, relational ag-
boys. However, overlap between the current work and that of Scarpa gression includes behaviors captured by measures of general aggression
with regard to the association between RSC and proactive aggression is but also excludes aggressive behaviors not intended to result in damage
not complete, as the current work did not find an association between to relationships.

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T. Armstrong et al. Biological Psychology 141 (2019) 44–51

A consideration of the current results in the context of the prior behavior (Bobadilla et al., 2012; Hubbard et al., 2002; Murray-Close
literature shows that it is difficult to specify the larger theoretical and et al., 2017; Murray-Close & Rellini, 2012; Pitts, 1997). These studies
practical implications of studies testing systematic differences between are situated in a larger literature that demonstrates that reactive and
males and females in the association between ANS activity and ag- proactive aggressive behavior, despite having a strong correlation, are
gressive behavior type. These studies vary with regard to ANS measure, indeed different. This larger literature now shows that despite to con-
stressor, and aggressive behavior type and typically do not directly siderable etiological overlap, reactive and proactive aggressive beha-
contrast results for males and females. Focusing on the current work, vior types have distinct social environmental, psychological, and phy-
we do find that when results for males and females are directly con- siological correlates (Baker et al., 2008; Brendgen et al., 2006; Card &
trasted differences across sex can emerge. These differences suggest that Little, 2006; Cima & Raine, 2009; Connor et al., 2004; Fite et al., 2009;
‘one size fits all’ models of aggression will not capture important dif- Vitaro et al., 2006). While this body of literature is convincing, in some
ferences across gender in the etiology of aggressive behaviors and call cases our understanding of the etiology of aggressive behavior type is
for additional research with a direct focus on sex differences in the role piecemeal. With this in mind, future work in this area may benefit from
of ANS activity in the explanation of aggressive behavior type. Direct a consideration of influence at each of these domains—social, psycho-
replication using similar or identical stressors, and similar or identical logical, and physiological—in the etiology of aggressive behavior type.
measures of ANS activity aggressive behavior may give critical in-
formation regarding the weight that should be given particular results. References
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