Empathy dysfunction in children and adolescents with disruptive behavior disorders
Minet de Wieda,⁎, Christine Gispen-de Wiedb, Anton van Boxtelc
aResearch Centre Adolescent Development, Utrecht University, P.O. Box 80140, 3508 TC Utrecht, The Netherlands
bRoosevelt Academy, Utrecht University, P.O. Box 94, 4330 AB Middelburg, The Netherlands
cDepartment of Psychology, Tilburg University, P.O. Box 90153, 5000 LE Tilburg, The Netherlands
a b s t r a c ta r t i c l ei n f o
Received 30 September 2009
Received in revised form 8 October 2009
Accepted 9 October 2009
Available online 17 October 2009
In this essay, we focus on empathy in children and adolescents with disruptive behavior disorders (DBD),
based on the assumption that lack of empathy is a risk factor for the development of DBD. We reflect on the
heterogeneity of DBD, the complex nature of the empathy construct, discuss empathy's role in aggression,
and review recent findings from studies on empathic skills in children and adolescents with DBD. Research
suggests that the mechanisms underlying empathy problems may be different for DBD subtypes. Individuals
with psychopathic tendencies may show a selective impairment in empathy with sadness and fear due to
abnormalities in neural circuits connected with the amygdala. Individuals without these tendencies may
show little empathy for a variety of reasons, such as hostile attributions, anxiety and/or poor regulatory
skills. Understanding more about the nature and causes of empathy dysfunction in DBD could aid in
identifying subtypes and help to improve prevention and intervention programs. Suggestions for future
research are made.
© 2009 Elsevier B.V. All rights reserved.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
DBD subtypes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Defining empathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Empathy and aggression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Modulating factors in empathic responding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Empirical evidence of empathy dysfunction in DBD individuals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.1.The psychopathic subtype . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.2.The non-psychopathic subtype . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.3.A multi-measure study on empathy in clinic-referred DBD boys . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Disruptive behavior disorders (DBD) can be classified according to
the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR)
(American Psychiatric Association, 2000) into oppositional defiant
disorder (ODD), and conduct disorder (CD). ODD is characterized by a
recurrent pattern of negativistic, defiant, disobedient, and hostile
behavior towards authority figures. Children or adolescents with ODD
often lose temper, argue with adults and deliberately annoy other
people. CD is a more severe type of behavioral disorder. The essential
feature of CD is a repetitive and persistent pattern of behavior in
which the basic rights of others or major age-appropriate societal
norms or rules are violated. Children or adolescents with CD often
initiate aggressive behavior and physical fights, they may lie and
deliberately destroy other people's property. ODD may be a
developmental precursor of CD in late childhood and adolescence,
which, in turn, may be a developmental antecedent of antisocial
personality disorder (APA, 2000). However, a suggested continuum of
disorders, either related to age, or severity, is far from reaching a point
of consensus both clinically and scientifically.
From a clinical perspective, children and adolescents with DBD are
thought to have little empathy and concern for the feelings and well-
European Journal of Pharmacology 626 (2010) 97–103
⁎ Corresponding author. Research Centre Adolescent Development, Faculty of Social
Sciences, Utrecht University, Heidelberglaan 1, P.O. Box 80140, 3508 TC Utrecht, The
Netherlands. Tel.: +31 30 253 7693; fax: +31 30 253 7731.
E-mail address: firstname.lastname@example.org (M. de Wied).
0014-2999/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
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being of others. From a scientific viewpoint, lack of empathy may be
regarded a risk factor to develop hostile, aggressive, or even violent
behavior (e.g., Feshbach, 1997). Meta-analytic studies show inverse
relationships between empathy and antisocial behaviors in normal
(Miller and Eisenberg, 1988) and forensic (Jolliffe and Farrington,
2004) populations. Relatively few studies have been conducted with
clinical samples (Lovett and Sheffield, 2007). Consequently, little is
known about the nature and causes of empathy dysfunction in the
group of children with ODD or CD, referred to as DBD.
Ingeneral,individuals withDBD constitutea heterogeneous group,
which is inherent to the DSM classification system. Subtyping is
important because of the need to differentiate between children who
are likely to stop their destructive behavior and those who will not.
The latter being possibly the ones that run the risk to develop
antisocial personality disorder or psychopathy in adulthood. Under-
standing more about the mechanisms underlying empathy deficits in
DBD individuals could aid in identifying subtypes and help to improve
prevention and intervention programs.
In this essay, we focus on empathy impairment in children and
adolescents with DBD. We will consider DBD subtypes, define the
construct of empathy, discuss its role in aggression, and review recent
findings from studies on empathic skills in children and adolescents
2. DBD subtypes
The DSM-IV-TR makes a distinction between children showing
conduct problems prior to the age of 10 years (childhood-onset type)
and those whose onset of conduct problems only starts at puberty
(adolescent-onset type). The childhood-onset type is more likely than
the adolescent-onset type to have persistent problems,and to develop
antisocial personality disorder in adulthood. Callous–unemotional
(psychopathic) traits designate a particular severe and violent
subgroup of antisocial children who show disruptive behavior already
early in development (child-onset type). Callous–unemotional traits
are an extension of the interpersonal-affective dimension of adult
psychopathy, and include lack of empathy and guilt feelings and low
emotional responsiveness (Frick et al., 1994; Lynam and Gudonis,
2005). Children and adolescents with callous–unemotional traits are
reward oriented, insensitive to punishment cues, lack emotional
responsiveness to distress cues and may show both reactive and
proactive (instrumental) aggression (see Frick and Marsee, 2007;
Frick andWhite, 2008 for researchreviews).DBD childrenwithout (or
low levels of) callous–unemotional traits may show less aggressive
behavior, and when they do, they show only reactive types of
aggression which are triggered by frustration and threat. They may
show high levels of anxiety, experience high levels of emotional
distress, and have problems regulating their emotions.
Viding and colleagues demonstrated that antisocial behavior in
children with callous–unemotional traits has high genetic loadings,
while such behavior in children with low levels of callous–unemo-
tional traits is under strong environmental influence (Viding et al.,
2005; Viding and Jones, 2008). Genes do not contribute to specific
antisocial behavior, but may disrupt the functioning of neural
networks including the amygdala (Blair, 2006a,b). The amygdala is
critically involved in aversive conditioning and the processing of
distress cues, especially fear-related information (Olsson and Phelps,
2007). Abnormalities in this area may hamper socialization. Brain-
imaging studies have demonstrated reduced amygdala activation
during processing of fearful facial expressions in DBD youth (Marsh,
Finger et al., 2008) and boys (Jones et al., 2009) with callous–
unemotional traits relative to healthy controls. De Brito et al. (2009)
and dorsal anterior cingulate cortex in conduct disordered boys with
callous–unemotional traits relative to healthy controls. These differ-
ences suggest a delayed maturation of cortical areas implicated in
Although no structural differences were found in the amygdala, the
amygdala has strong functional connections with these cortical areas.
Abnormalities in these networks may reduce activity in the stress
response systems, that is, the autonomic nervous system and
hypothalamo–pituitary–adrenal system (Lane et al., 2009). Many
researchers have examined the stress response systems, based on the
idea that children with DBD are underaroused and need their
behavior to reach some level of arousal and corresponding stress
hormone levels to “feel good” or be rewarded (e.g., Ortiz and Raine,
2004; van Goozen et al., 2007). Low resting heart rate is one of the
best replicated biological markers of aggressive and antisocial
behavior (Lorber, 2004; Ortiz and Raine, 2004; Raine, 2002). Low
activity in the hypothalamo–pituitary–adrenal system is a predispos-
ing factor in high risk groups (Sondeijker et al., 2008), and has been
observed in children with callous–unemotional traits (Loney et al.,
2006). Thus, a distinction can be made in antisocial behavior based on
the presence of callous–unemotional traits, where children with
callous–unemotional traits are emotional under-reactive due to
abnormalities in circuits connected to the amygdala (fearless type).
Children without (or low levels of) callous–unemotional trait are
emotionally (over-) reactive, and more sensitive to environmental
influences (fearful type).
3. Defining empathy
Empathy, generally defined as the ability to understand and share
another's emotional state (Cohen and Strayer, 1996; Davis, 1996;
Feshbach, 1997; Hoffman, 2000) is a complex multi-component
phenomenon, encompassing trait empathy (empathic tendencies of
an individual), state empathy (empathic reactions elicited in concrete
situations), primitive (affective) and more sophisticated (cognitive)
empathy-related processes. In the literature a distinction is often
made between cognitive empathy, affective empathy, and primitive
or motor empathy. Cognitive empathy refers to the cognitive
awareness of another person's internal state. Perspective-taking,
mentalizing, or theory of mind are considered aspects of cognitive
empathy. Affective empathy involves the vicarious experience of
emotions consistent with those of others. Empathy is distinguished
from two empathy-related responses, that is, sympathy and personal
distress (Eisenberg, 2000). Empathy involves a matching of emotions
between the observer and target, that is, feeling with another person.
With further cognitive processing, empathy may turn into either
sympathy (an other-oriented emotion) or personal distress (a self-
focused emotion), or some combination. Sympathy consists of
feelings of sorrow or concern for the target, that is, feeling for another
person. In contrast, personal distress is an aversive reaction which
may consist of feelings of discomfort or anxiety, thus feeling by the
state of the other (Batson, 2009). Empathy, sympathy, and personal
distress are closely related constructs and often part of the same
Primitive or motor empathy refers to automatic mimicry process-
es. People tend to mimic emotional facial expressions (Dimberg,
1990; Dimberg et al., 2000), and such mimicry processes are thought
to be a determinant of emotional contagion (Hatfield et al., 1994,
2009). Current researchers agree that motor mimicry is an innate
capacity which contributes to the development of empathy in the
preverbal years, and continues to play a role past childhood (Hoffman,
2000; Meltzoff and Decety, 2003; Preston and de Waal, 2002).
Brain-imaging studies suggest that distinct but interacting brain
structures are involved in cognitive and affective empathy (see
Shamay-Tsoory, 2009; Völlm et al., 2006). Perspective-taking pro-
cesses and theory of mind may involve prefrontal brain areas,
including the ventromedial prefrontal cortex and lateral orbitofrontal
cortex, and temporal areas, including the superior temporal sulcus
M. de Wied et al. / European Journal of Pharmacology 626 (2010) 97–103
and temporal pole. Affective empathy primarily involves the insula
and limbic structures, including the amygdala and anterior cingulate
cortex. In patients with selective brain lesions, Shamay-Tsoory et al.
(2009) found a double dissociation between areas involved in
cognitive empathy (ventromedial prefrontal cortex) and affective
empathy (inferior frontal gyrus).
The mirror neuron system is proposed to be involved in automatic
mimicry responses. Initial studies with primates localized the mirror
neuron system in premotor areas, including the inferior frontal gyrus,
and parts of the inferior parietal lobe (see Iacoboni and Dapretto,
2006; Rizzolatti and Craighero, 2004 for reviews). Studies in humans
suggest that the mirror neuron system extends to the superior
temporal sulcus and other areas in the prefrontal and parietal cortex.
It is connected to the limbic system by the insula. The mirror neuron
system enables understanding experiences and intentions of others
through direct simulation of observed actions and emotional expres-
sions (Iacoboni and Dapretto, 2006). A typical example is empathy for
pain. Experiencing pain in oneself and observing pain in someone else
activates similar structures which are related to the affective but not
the sensory aspect of pain, specifically the anterior cingulate cortex
and anterior insula (Botvinick et al., 2005; Singer et al., 2004).
Likewise,observingfacesofdisgust andexperiencing disgust activates
similar sites in the anterior cingulate cortex and anterior insula
(Wicker et al., 2003). The cognitive and affective empathy networks
may also include the mirror neuron system in premotor areas (Carr
et al., 2003). As such, it can be understood that the different
components of the construct ‘empathy’ may be selectively impaired
with consequent differences in behavioral problems and, subsequent-
ly, treatment options.
4. Empathy and aggression
In general, empathy is thought to promote positive behavior such
as helping (Eisenberg and Miller, 1987), and to prevent or reduce
antisocial behavior, including aggression and delinquency (Jolliffe and
Farrington, 2004; Miller and Eisenberg, 1988). The inhibitory effect of
empathy may apply to both proactive and reactive aggression
(Feschbach and Feschbach, 2009). Feshbach's (1997) cognitive-
affective model of empathic behavior identifies three adaptive skills
for children and adults: (1) the ability to discriminate affective cues in
others (2) perspective-taking, and (3) affective responsiveness. The
ability to discriminate and label the emotions of others is a
precondition to show consideration with other's needs and desires.
The second component of empathy, perspective-taking, is a more
advanced cognitive skill that should promote positive problem
solving. Adopting the perspective of the other person in a conflict
situation may lead to a better understanding of the other's position,
preventing destructive acts and fostering productive ones. The third
component of empathy, affective responsiveness comes into play
when aggressive acts cause pain and distress in the victim. The
observation of distress in the victim may elicit empathic distress,
which should function as an inhibitor of aggression.
Blair's (1995, 2001, 2006a) violence inhibition mechanism model
offers an explanation from an evolutionary perspective. Starting from
ethologists' observations that most social animals possess mechan-
isms for the control of aggression, Blair proposed that humans might
possess a functionally analogous mechanism, that is, a violence
inhibition mechanism. The violence inhibition mechanism is selec-
tively activated by the display of distress cues (expressions of fear and
sadness), which functions as a human submission response. Activa-
tion of the violence inhibition mechanism increases autonomic
activity and activation of the threat response system, which initiates
a withdrawal response, resulting in the interruption of aggressive
behavior. Poor functioning of the violence inhibition mechanism is
attributed to abnormalities in the limbic system, specifically the
amygdala. The violence inhibition mechanism model predicts that
amygdala dysfunction may result in the development of antisocial
behavior seen particularly in psychopathic individuals. Children with
lesions in this area may learn to use aggression to achieve their goals
because they are reinforced (not punished) for their aggressive acts.
They may develop instrumental aggression, accordingly. Reactive
aggression is associated with abnormalities in the orbitofrontal
cortex, whose primary function is to regulate activities in the stress
response systems. When regulation fails, the systems may become
over-responsive, which may lead to impulsive/reactive aggression
(Blair, 2006a,b; Blair et al., 2005).
5. Modulating factors in empathic responding
Adequate empathic responding requires self–other differentiation
and emotional control. Eisenberg and colleagues (Eisenberg et al.,
1994; Eisenberg and Eggum, 2009) have stressed the importance of
emotion regulation in empathic responding. Individuals who are
emotionally responsive but poor in regulatory skills are at risk to
experience high levels of arousal when witnessing others in distress,
and to experience personal distress. Well-regulated individuals are
thought to maintain optimal levels of empathic arousal and to
experience sympathy, which reduces aggression and promotes
prosocial behavior. Those experiencing personal distress become
self-focused and motivated to reduce their own rather than the
victim's distress. Research conducted by Eisenberg and colleagues
(reviewed in Eisenberg et al., 1998) supports the hypothesis that
empathy-related responding is linked to emotion regulation. Taking a
detached observer position is one way to regulate distress, and to
prevent empathic overarousal in empathic individuals. Deficits in
self–other distinctiveness may impair empathic responding, accord-
ingly (e.g., Decety and Lamm, 2009; Lamm et al., 2007). At the level of
the brain, the right temporoparietal junction is a key region in self–
other differentiation (see Decety and Lamm, 2009). Frontal brain
areas, including orbitofrontal cortex and anterior cingulate cortex, are
important structures in the regulation of emotional behavior
(Ochsner and Gross, 2005).
Studies with healthy individuals further suggest that empathy may
depend on context or interpersonal factors, such as similarity between
Englis (1989) manipulated observer's expectations of cooperation or
competition, and found that cooperation promotes empathy, whereas
competition promotes counter-empathy, that is, an opposite valenced
emotion. Similarly, Zillmann and Cantor (1977) demonstrated that
healthy children experience concordant emotions when they like the
person being observed, and discordant emotions when they dislike the
person being observed. A recent brain-imaging study conducted by
male and female students watched someone they liked or disliked
experiencing pain. In agreement with earlier studies, pain-related
empathic responses were observed in the anterior insula and anterior
cingulate cortex when seeing a likeable person in pain. For men (not for
women), these empathy-related responses were significantly reduced
when they witnessed a disliked person in pain. Interestingly, this effect
was accompanied by increased activation in reward-related areas (left
ventral striatum/nucleus accumbens). These findings suggest that
empathic sensitivity can be turned on or off, depending on whether
we are among friends or facing foes.
6. Empirical evidence of empathy dysfunction in DBD individuals
6.1. The psychopathic subtype
Although lack of empathy is long considered essential to
psychopathy (Hare, 1993), empirical data are rather limited. Among
M. de Wied et al. / European Journal of Pharmacology 626 (2010) 97–103
the relatively few studies that examined empathic skills in children
and adolescents with psychopathic traits, most have focused on the
ability to discriminate affective cues (the first factor in Feshbach's
model). Individuals with psychopathic tendencies are selectively
impaired in the recognition of fearful and sad facial expressions (Blair
and Coles, 2000; Blair et al., 2001; Dadds et al., 2006; Fairchild et al.,
2009; Stevens et al., 2001), although one study found that children
with psychopathic tendencies are more accurate than controls in
identifying fearful expressions (Woodworth and Waschbusch, 2007).
The results demonstrate that individuals with psychopathic tenden-
cies are not impaired for all expressions. They are particularly
impaired in recognizing fearful and sad expressions.
There is little evidence that individuals with psychopathic traits
are impaired in cognitive role-taking (the second factor in Feshbach's
model) (see Anastassiou-Hadjicharalambous and Warden, 2008a;
Blair, 2007, 2008), although Pardini et al. (2003) found a negative
relationship between callous–unemotional traits and both disposi-
tional role-taking and empathic concern in adjudicated youth. Some
studies examined emotional responsiveness in children with psycho-
pathic tendencies (the third factor in Feshbach's model). Blair (1999)
demonstrated reduced electrodermal responses to distress cue
pictures in boys with psychopathic tendencies relative to controls.
Anastassiou-Hadjicharalambous and Warden (2008b) examined
heart rate responses to an empathy-inducing film clip involving
fear. CD children with callous–unemotional traits showed less heart
rate change than CD-only or healthy controls. Overall, findings
demonstrate that individuals with psychopathic tendencies are
emotionally under-reactive to distress cues (sadness and fear). The
selective impairment in the processing of sad and fearful expressions
has been attributed to amygdala dysfunction, proposed to be the core
deficit in psychopathy (e.g., Blair, 2007).
6.2. The non-psychopathic subtype
Empathy deficits proposed for the non-psychopathic subtype may
stem from multiple sources such as negative sentiments, hostile
attributions, anxiety and/or poor emotion regulation. For example,
Evans et al. (2002) argued that children with DBD do not completely
lack the capacity of feeling empathy, but show little empathy because
they tend to interpret social cues in ways that may elicit feelings of
threat or anger. The tendency to misperceive the intentions of others
as more hostile and threatening than is the case, is listed as an
associated feature in the DSM-IV-TR classification of CD (APA, 2000).
This observation is given support by studies demonstrating that
aggressivechildrenare inclinedto makehostileattributions(Dodgeet
al., 1990; Orobio de Castro et al., 2002). Hostile attributions and
negative sentiments may reduce empathic responding as outlined
above. Accordingly, it is quite likely that DBD children respond less
empathically, not because they completely lack the capacity of feeling
empathy, but because their negative attitudes preclude empathic
Alternatively, it is possible that DBD individuals show reduced
empathy because they are highly reactive to other's distress, and have
high-frequency component of heart rate variability) are linked to a
variety of psychiatric disorders, including depression, anxiety and
parasympathetic activation, as apparent form measures of respiratory
sinus arrhythmia, has been observed in children and adolescents with
DBD (Beauchaine, 2001; Beauchaine et al., 2001, 2008), also in
combination with low sympathetic activation (Beauchaine et al.,
2007; Mezzacappa et al., 1997). Problems in emotion regulation can
render a child particularly susceptible to becoming overaroused in
response to other's distress, leading to self-focused attention and
personal distress. Accordingly, it is quite possible that DBD individuals
show little empathy, not because they are under-responsive to distress
cues (as seen in psychopathic individuals), but because they are over-
responsive to negative stimuli. Frontal brain areas are involved in
emotionregulation,andabnormalities in theseareasmaybeimplicated
in empathy problems seen in DBD individuals (Sterzer et al., 2005,
Cohen and Strayer (1996) were the first to establish empathy
impairments in clinic-referred CD adolescents, using self-report
measures of state and trait empathy. State empathy was assessed by
respondent's emotional and cognitive responses to empathy-inducing
video-vignettes. Trait empathy was assessed by self-report question-
naires of affective and cognitive empathy. The study demonstrated
trait empathy. More recently, Marsh, Beauchaine and Williams (2008)
included autonomic responses and judgment of facial expressions as
indexes of empathy in their research on empathy in school-aged DBD
boys. They found no significant differences in skin conductance level,
cardiac pre-ejection period, respiratory arrhythmia or facial respon-
siveness between DBD boys and controls during exposure to a video-
vignette portraying a child being depressed. However, DBD boys
showed less correspondence across different response systems than
control boys, which illustrates the importance of using multiple
measures in studies on empathy in DBD children.
We used a multi-measure approach in our study on empathy in
school-aged DBD boys. We focused on affective empathy and included
self-report indexes of state and trait empathy, as well as autonomic
and facial indexes of state empathy. We will briefly summarize the
6.3. A multi-measure study on empathy in clinic-referred DBD boys
The boys participating in our study were all aged between 8 and
12 years. DBD boys were recruited from inpatient and day-treatment
units, and met the criteria for ODD or CD as set out in the DSM-IV-TR
(APA, 2000). The healthy control boys were recruited from regular
schools. Parent- and teacher-ratings of children's behavior problems
were assessed. Relative to controls, DBD boys obtained significantly
higher scores on all measures of externalizing behaviors, as well as on
measures of internalizing behaviors (withdrawn and anxious/
depressed). We also examined basal patterns of autonomic activity
in a subsample, and found higher resting heart rate (reflecting high
arousal) and lower respiratory sinus arrhythmia (reflecting poor
emotional control) in DBD boys compared to controls. The overall
pattern suggests that our DBD group belongs to the temperamentally
more fearful, rather than fearless subtype (de Wied et al., 2009). All
boys were individually tested in a test room at the clinic according to a
basal autonomic activity). Next, they were shown dynamic happy and
angry facial expressions (to assess facial mimicry responses), followed
by empathy-inducing film clips (to assess verbal and physiological
responses of empathy). The verbal and physiological data were
presented in different manuscripts.
In the first study (de Wied et al., 2005), we examined state and
trait empathy. Trait empathy was measured by a self-report
questionnaire of affective empathy for children. State empathy was
assessed by children's emotional–cognitive responses to six empathy-
inducing video-vignettes. The video-vignettes were assembled for use
in our study, and involved either negative emotions (sadness and
anger) or positive emotions (happiness). In line with predictions and
previous findings (Cohen and Strayer, 1996), DBD boys showed
deficits in both trait and state empathy. Regarding empathic
responding to the separate emotions, we found that DBD boys
reported less empathy in relation to negative emotions (sadness and
anger), but no less empathy in relation to positive emotions
(happiness). DBD boys reported less empathy to each and every
M. de Wied et al. / European Journal of Pharmacology 626 (2010) 97–103
sadness vignette. However, both DBD boys and controls reported
significantly higher levels of empathy when they viewed a baby bear
in distress than when they viewed a boy or girl in distress. These
findings confirm that stimulus characteristics affect children's
empathic responding, and demonstrate that DBD boys do not
completely lack the capacity of feeling empathy.
In the second study with a subsample (de Wied et al., 2009), we
examined physiological correlates of empathy. Heart rate, and
electromyographic responses in the zygomaticus major (cheek) and
corrugator supercilii (eyebrow) muscles were assessed during
exposure to the same empathy-inducing vignettes. Autonomic and
facial indexes of empathy have often been used in studies on
children's empathy (Zhou et al, 2003). However, we introduced facial
electromyography to examine facial responsiveness. Facial electro-
myography is a sensitive measure which allows for a better detection
of facial muscle activity than the visual coding techniques that are
generally used. Positive stimuli, including happy facial expressions,
typically evoke an increase in zygomaticus muscle activity, whereas
negative stimuli, including angry facial expressions, evoke and
increase in corrugator muscle activity (Larsen et al., 2003). In our
study, the positive and negative clips evoked this typical electromyo-
graphic response pattern in normal controls. Relative to controls, DBD
boys showed a smaller increase in corrugator muscle activity during
negative emotions (sadness and anger), but not smaller zygomaticus
muscle activity during happiness. Also, DBD boys showed less heart
rate reduction (reflecting sympathy/outward focus of attention)
during sadness but not during anger or happiness. These findings
reveal subnormal electromyographic and heart rate responses for
DBD boys in relation to negative emotions (sadness in particular) but
not to positive emotions.
In the third study with the same subsample (de Wied et al., 2006),
and controls. In this study respondents were exposed to 5-s moving
pictures showing a male model producing dynamic angry or happy
facial expressions. Facial electromyographic activity in the zygomaticus
stimuli. Based on observations that DBD boys are weak empathizers we
expected them to be poor mimickers as well. Overall, the happy and
angry facial expressions evoked distinct facial electromyographic
patterns, with enhanced zygomaticus muscle activity to happy expres-
sions, and enhanced corrugator muscle activity to angry expressions.
Dimberg, 1990). Interestingly, facial mimicry responses to angry (not
happy) facial expression were subnormal in DBD boys, suggesting that
DBD boys are selectively impaired in an early component of emotional
On balance, the data obtained in our study showed that the DBD
group, identified by high resting heart rate (reflecting high arousal),
and low levels of resting respiratory sinus arrhythmia (reflecting poor
emotional control), is impaired in empathy with negative (not
positive) emotions. Relative to controls, DBD boys reported less
empathy with negative (not positive) emotions in our first study. The
self-reports were confirmed by the physiological response patterns
obtained in our second study, and by facial mimicry responses in our
In this essay we discussed empathy in children and adolescents
with DBD, based on the assumption that lack of empathy is a risk
factor for developing DBD. Empathy is thought to inhibit aggression
through perspective-taking andempathic concern. Perspective-taking
is likely to influence how the provocation is interpreted which may
lead to reduced anger. When it comes to aggression, the observation
of the victim's pain and distress may evoke empathic distress in
emotionally responsive individuals. Whether empathic distress leads
to sympathy (an other-oriented emotion) or personal distress (a self-
focused emotion) depends, in part, on self–other differentiation and
regulatory skills. Individuals who are not emotionally responsive (e.g.,
psychopathic individuals) or not emotionally involved (by detest or
lack of interest) may show no empathic distress, and therefore no
cessation of aggression. At the level of the brain, the limbic system
(amygdala) and frontal brain areas (orbitofrontal cortex and anterior
cingulate cortex) are critically involved in the empathy process and
the development of aggressive behavior.
The hypothesis that empathy inhibits aggression implies that
aggressive behavior may be reduced by enhancing empathic skills in
antisocial individuals. Research suggests that training programs
aimed to strengthen empathic skills are effective in reducing
antisocial behavior in healthy children. (see Feshbach, 1997;
Feschbach and Feschbach, 2009). However, DBD is a heterogeneous
disorder and DBD subtypes are likely to require different approaches
to intervention. Based on theoretical and empirical evidence, it is
postulated that the mechanisms underlying empathy problems in
DBD children with callous–unemotional traits (fearless type) may be
different from those encountered in DBD children without these traits
(fearful type). Children with psychopathic tendencies may show
selective impairments in empathic sadness and fear, due to abnor-
malities in neural circuits involving the amygdala (Blair, 2007, 2008;
Blair et al., 2005). It is speculated that DBD children without these
tendencies may show little empathy for a variety of reasons. One such
reason may be that they harbor suspicions or evil thoughts against
their victim, which precludes empathic responding. Another reason
may be that they are poor in regulatory skills. Children who cannot
adequately regulate their emotions are at risk to become empathically
overaroused and to experience personal distress. Although empathy
dysfunction in psychopathic individuals has received far more
research attention than empathy dysfunction in non-psychopathic
individuals, the empathy patterns sketched above for DBD subtypes
are highly hypothetical and need further examination.
between subtypes. The study produced several interesting findings.
First, resultsshowedthatDBD boys belongingtothe fearful, rather than
the fearless, subtype are selectively impaired in empathy with negative
(not positive) emotions. It is important to note in this context that
selective impairments in the processing of negative stimuli have also
been established in studies with healthy boys (Eisenberg et al., 2001;
Feshbach, 1982; Zhou et al., 2002), and is thus not specific to DBD boys.
Second, the results showed that the level of impairment depends on
stimulus characteristics, suggesting that DBD boys do not completely
lack the capacity for feeling empathy.
Clearly, more in-depth research is needed to gain insight into the
natureand causes of empathyimpairment in childrenandadolescents
withDBD. Giventhe complex natureof the empathyconstruct andthe
heterogeneity of DBD we need to adopt a multi-measure approach
and describe our samples carefully. One useful approach would be to
examine empathic response patterns in relation to a broad range of
emotions. One may possibly find (1) a selective impairment in
empathy with sadness and fear if amygdala dysfunction is a factor,
(2) a selective impairment in empathy with negative (not positive)
emotions if emotion-dysregulation is a factor (i.e., frontal brain areas
implicated), or (3) reduced empathy with all emotions if hostility is a
factor (i.e., context driven).
New instruments are needed to examine deficits at different levels of
empathic functioning. So far, self-report measures are most commonly
used for assessing empathy in children and adolescents (Zhou et al.,
2003). However, early empathy deficits are unlikely to be validly
assessed using self-report measures. Facial electromyography may be
considered a promising new technique in the study of children's
empathy. Facial electromyography is a highly sensitive measure of facial
M. de Wied et al. / European Journal of Pharmacology 626 (2010) 97–103
procedures are not dependent on introspective and verbal skills and
could thus be used to study empathy dysfunction in children and
adolescents from different cultural backgrounds.
We have successfully applied facial electromyography in our study
on empathy in DBD boys. The findings from this first study show that
fundamental processes can be studied in children with rather simple
techniques. In clinical practice it is often difficult to discriminate
disordered children with psychopathic traits from those without such
traits because of the behavioral similarities between the two groups.
For adequate diagnosis, fundamental differences in their empathic
function may become significant. Facial electromyography might
prove to be an objective instrument in this respect to measure change
and outcome in empathy training programs, and a useful tool for
diagnostic purposes in clinical practice.
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