Introduction
Disruptive behavior disorders (DBD), including oppositional defiant disorder (ODD) and conduct disorder (CD), are the most prevalent psychiatric disorders in children and adolescents (e.g., Ford et al.
2003; Verhulst et al.
1997). The
Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR, American Psychiatric Association
2000) defines ODD as a recurrent pattern of negativistic, defiant, disobedient, and hostile behavior towards authority figures. CD is a more severe type of disorder, characterized by a repetitive and persistent pattern of behavior in which the basic rights of others or major age-appropriate societal norms or rules are violated. 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 (APD) which can be diagnosed from age 18 (APA
2000).
Callous-unemotional (CU) traits identify an important subgroup of antisocial youths in forensic (Vaughn et al.
2008), clinical (Christian et al.
1997), and community samples (Frick et al.
2003,
2005). Antisocial children and adolescents with CU traits show particular high rates of conduct problems, delinquency and police contacts (see also Frick and White
2008 for a research review). Callous-unemotional traits are an extension of the interpersonal-affective dimension of adult psychopathy—a special case of APD—and include a lack of empathy, lack of guilt and low emotional responsiveness (Frick and Hare
2001). Callous-unemotional traits in childhood have high genetic loadings (Viding et al.
2005), and are associated with persistent criminal behavior (Pardini and Fite
2010) and measures of psychopathy in adulthood (Burke et al.
2007).
In preparation to the fifth edition of the DSM it is proposed to include CU traits as a specifier/subtype for the diagnosis of CD (Frick and Moffit
2010; Scheepers et al.
2011). Although lack of empathy is a defining feature of callous-unemotional traits, surprisingly few studies have directly examined empathy in conduct disordered youths with CU traits. The primary goal of the present study is to examine empathy-related responding in DBD male adolescents with high vs low CU traits and age-matched healthy controls.
Empathy, generally defined as the ability to understand and share another’s emotional state (Davis
1996; Hoffman
2008), is a complex multi-component phenomenon, encompassing trait empathy (empathic tendencies of an individual), state empathy (empathic reactions elicited in concrete situations), cognitive empathy (understanding another person’s emotions) and affective empathy (sharing another person’s emotions). A distinction is often made between different types of affective responding, that is, empathy, sympathy and personal distress (Eisenberg and Eggum
2009). Empathy involves a matching of emotions between the observer and target, that is, feeling
with another person. Sympathy consists of feelings of sorrow or concern for the target, thus, feeling
for another person. In contrast, personal distress is an aversive reaction, which may consist of feelings of discomfort or anxiety.
Empathy dysfunction proposed for psychopathic individuals is thought to be related to abnormalities in the limbic region, especially the amygdala (Blair
2005,
2007). The amygdala is involved in aversive conditioning and the processing of distress cues, especially fear-related information (Olsson and Phelps
2007). Lesions in this area may lead to a selective impairment in empathy with fear, sadness and possibly disgust (Blair
2007). Recent brain imaging studies show reduced amygdala activation during processing of fearful facial expressions in DBD individuals with high CU traits relative to healthy controls (Jones et al.
2009; Marsh et al.
2008). Empirical studies on facial affect recognition (Blair et al.
2001; Fairchild et al.
2009; Stevens et al.
2001) further support that children and adolescents with DBD
and CU traits have selective impairments in the recognition of fearful and sad expressions (not anger, surprise or happiness). Inverse relationships between CU traits and fear recognition have also been established in studies with community samples of antisocial children and adolescents (Dadds et al.
2006,
2008). Findings from these and other studies (e.g., Dadds et al.
2011) suggest that fear blindness in children with CU traits is in part due to impaired attention to the eye region of the face, which may also relate to amygdala dysfunction.
Despite the considerable amount of research on facial affect recognition in psychopathic individuals, there has been little attention given to empathy-related responding within more complex empathy-inducing settings. Two studies have recently used self-report measures to examine empathic dysfunction in boys with emotional and behavioral difficulties (Jones et al.
2010), and school-aged children with conduct disorder (Anastassiou-Hadjicharalambous and Warden
2008a). Both studies demonstrate that those with high CU traits are particularly impaired in affective empathy, but relatively competent in cognitive perspective taking abilities. In an early study, Blair (
1999) examined autonomic (electrodermal) responses to distress cue pictures in school-aged boys with emotional and behavioral difficulties. Boys with psychopathic tendencies showed less electrodermal responsiveness than those without these tendencies or healthy controls. Anastassiou-Hadjicharalambous and Warden (
2008b) examined verbal and autonomic (heart rate) responses to a videotaped event involving fear in a sample of school-aged children with CD. In line with predictions, high CU children showed less heart rate change than low CU children or controls. Self-reports were not completely consistent with autonomic responses: both CD groups reported less empathic distress than healthy controls and obtained lower scores on a questionnaire measure of affective empathy. Hence, autonomic response patterns (
not self-reports) support distinct empathy deficits across subgroups of children with severe behavior problems. We found no studies replicating these findings in subgroups of DBD adolescents.
The current study adopts a multi-measure approach to examine patterns of affective empathy in DBD adolescents with high vs low CU traits and healthy controls. Respondents were exposed to six empathy-inducing film clips involving either negative (sadness and anger) or positive (happiness) emotions. During exposure, facial electromyographic (EMG) activity in the zygomaticus major (cheek) and corrugator supercilii (eyebrow) muscle regions and heart rate (HR) responses were monitored. After each film clip, respondents were asked about the emotions expressed by the protagonist and the emotions they had experienced themselves.
Facial EMG procedures are commonly used to examine emotional contagion in adults. Positive stimuli, including facial displays of happiness, typically evoke an increase in zygomaticus activity, whereas negative stimuli, including facial displays of sadness and anger, evoke an increase in corrugator activity (e.g., Dimberg
1990; Larsen et al.
2003; Lundqvist and Dimberg
1995). Studies with healthy students show that this typical EMG pattern is less pronounced in low empathizers (Sonnby-Borgström
2002, Sonnby-Borgström et al.
2003; Westbury and Neumann
2008).
Heart rate responses have often been used to differentiate between sympathy and personal distress (e.g., Eisenberg and Fabes
1990). In normal persons, passive exposure to film clips eliciting sadness, anger, or happiness is generally associated with HR deceleration (e.g., Kreibig et al.
2007; Tsai et al.
2000; Waldstein et al.
2000), possibly reflecting an orienting/attention response. Sympathy or empathic concern is an other-oriented emotion, involving an observer perspective. This state has been associated with HR deceleration. In contrast, personal distress is a self-focused emotion, which has been associated with HR acceleration (Eisenberg and Fabes
1990; Zhou et al.
2003).
While empathy problems proposed for psychopathic individuals may be linked to amygdala dysfunction, empathy problems proposed for the non-psychopathic DBD subtype may stem from multiple sources, including hostility, anxiety and/or emotion regulation dysfunction (e.g., de Wied et al.
2010). Individuals who are emotionally responsive but poor in regulatory skills are at risk to experience personal distress and to become self-focused when witnessing another person in distress (Eisenberg and Eggum
2009). They may show little impairment in euphoric empathy because sharing positive emotions may reduce rather than enhance distress. Recent studies with DBD boys (de Wied et al.
2005,
2009) suggest that those belonging to the more fearful subtype show a selective impairment in empathy with negative (
not positive) emotions. Selective impairments in dysphoric (
not euphoric) empathy have also been established in studies with antisocial boys from normal populations (Eisenberg et al.
2001; Zhou et al.
2002).
Based on these findings along with findings suggesting that antisocial individuals are weak empathizers (see Lovett and Sheffield
2007; Miller and Eisenberg
1988), we hypothesize that DBD adolescents with low CU traits show less empathy (i.e., report less empathy, show less facial responsiveness and less heart rate reduction) than controls, especially in relation to the film clips involving negative emotions (sadness and anger). Based on theory and research suggesting that those with high CU traits are selectively impaired in the processing of sadness and fear (e.g., Blair
2007), we hypothesize that DBD adolescents with high CU traits will show a selective impairment in empathic responsivity to the film clips involving sadness (
not anger or happiness). Based on evidence suggesting that high CU individuals may lack emotionally responsiveness to negative stimuli (see Frick and White
2008), we hypothesize that DBD adolescents with high CU traits will show stronger impairments in empathic sadness than those with low CU traits.
A secondary goal of the present study is to examine basal autonomic function in DBD adolescents with high and low CU traits and normal controls. Numerous studies show basal autonomic disturbances in children with externalizing disorders, predominantly low resting HR (see Lorber
2004; Ortiz and Raine
2004 for meta-analyses). Low resting HR, thought to be driven by sympathetic underactivation, is one of the best replicated biological markers of aggressive and antisocial behavior (Ortiz and Raine
2004; Raine
2002). Nevertheless, a small number of studies have demonstrated high resting HR in clinic-referred DBD boys (Cole et al.
1996; de Wied et al.
2009; Zahn and Kruesi
1993).
Reduced parasympathetic activation (or cardiac vagal tone) indexed by reduced heart rate variability (HRV) or respiratory sinus arrhythmia (RSA, i.e., the high-frequency component of HRV), has been associated with a variety of psychiatric disorders, including depression, anxiety and aggression (Beauchaine
2001; Thayer and Lane
2000). Reduced cardiac vagal tone has been observed in children and adolescents with DBD (Beauchaine
2001; Beauchaine et al.
2001,
2008; de Wied et al.
2009), also in combination with low sympathetic activation (Beauchaine et al.
2007; Mezzacappa et al.
1997). To identify basal patterns of autonomic activity in the current group of DBD adolescents, resting HR and resting RSA were assessed during a 5-min relaxation video prior to the emotional film clips.
Discussion
The main goal of this study was to examine emotional empathy in subgroups of DBD male adolescents and healthy controls. To our knowledge, this is the first study that examined autonomic activity together with verbal and facial EMG responses to different target emotions in DBD adolescents with high versus low CU traits. The study produced some interesting findings. First, in agreement with expectations, DBD adolescents with high CU traits showed significantly lower levels of empathic sadness than healthy controls across all response systems. Specifically, high CU respondents reported less empathy, showed less facial responsiveness, and less HR change from baseline during sadness than controls. Different from expectations, high CU respondents also reported less empathic happiness than controls. Second, consistent with conceptualizations of CU traits, the CU (
not I/CP) factor was associated with empathy-related responses, including autonomic reactivity during sadness. Third, autonomic (
not verbal nor facial) reactions to sadness produced distinct differences between DBD subgroups. In agreement with expectations, DBD adolescents with high CU traits showed significantly less HR change from baseline during sadness than those with low CU traits. Our findings are consistent with earlier findings demonstrating reduced autonomic response patterns during distress cue pictures (Blair
1999) and empathy-inducing film clips involving fear (Anastassiou-Hadjicharalambous and Warden
2008b) in antisocial children with high CU traits relative to those with low CU traits or controls. The results have been interpreted within Blair’s (
1995,
2006) Violence Inhibition Mechanism (VIM) model, which posits that reduced autonomic responses to distress cues may result from deficits within the VIM. The VIM is thought to be an innate mechanism for the control of aggression, typically activated by the sad and fearful expressions of others. Activation of the VIM results in autonomic arousal and the interruption of on-going (aggressive) behavior. Deficits within the VIM – resulting from a more general amygdala dysfunction – may lead to the development of aggressive behavior particularly seen in psychopathic individuals. Results of the current study are consistent with the VIM model by showing subnormal levels of HR reactivity during sadness in adolescents with high CU traits.
Heart rate reactivity reflects sympathetic and parasympathetic activation mediated by limbic and prefrontal structures, including the anterior cingulate cortex (ACC) (Bush et al.
2000; Devinsky et al.
1995; Medford and Critchley
2010; Thayer and Lane
2000). ACC is connected to anterior insula and both structures are involved in understanding emotional experiences of others (Singer et al.
2009), for example, in generating empathy when seeing someone in pain (Gallese et al.
2004). Reduced ACC responses to negative affective pictures have been observed in conduct disordered adolescents compared to controls (Stadler et al.
2007; Sterzer et al.
2005). Ventral and rostral areas of ACC have affective functions and are involved in the monitoring and regulation of social emotional responses (Adolphs
2003). Structural or functional changes in rostral ACC combined with changes in orbitofrontal cortex may cause prominent changes in social behavior and may lead to antisocial responses (Devinsky et al.
1995). An increased concentration of grey matter in medial orbitofrontal cortex, and in rostral and dorsal ACC has been observed in boys with conduct disorder and CU traits compared to healthy controls (de Brito et al.
2009), suggesting a delayed maturation of cortical areas implicated in processing of affective stimuli and the experience of empathy. Hence, subnormal HR reactivity to sadness by DBD adolescents with high CU traits may possibly relate to abnormalities in prefrontal brain regions including the ACC.
The current group of DBD adolescents with low CU traits showed a more diffuse pattern of empathy dysfunction. Relative to controls, they reported less empathic happiness, and showed deficits in facial responsiveness to both sadness and happiness. No impairments were observed in HR measures of empathic sensitivity. The data are not completely consistent with previous work (de Wied et al.
2005,
2009) suggesting that DBD boys are selectively impaired in empathy with negative (
not positive) emotions. One possible explanation for the inconsistency is that DBD adolescents constitute a more heterogeneous group than DBD children because an older group is more likely to include both persons with adolescence-limited antisocial behavior and persons with early-onset pathways (Moffitt
1993). Alternatively, the variability of results could be due to differences in stimulus materials and/or developmental processes. For example, increasing testosterone levels in males at puberty and/or age-related changes in frontal lobe maturation are likely to affect empathic behavior (e.g., Decety
2010; Hermans et al.
2006).
Basal Autonomic Function
A second goal of the present study was to examine basal autonomic function in subgroups of DBD adolescents and controls. Resting HR was not significantly different between the three groups but resting RSA was significantly lower in DBD adolescents with high CU traits than in controls. Also, resting RSA tended to be lower in DBD adolescents with high CU traits compared to those with low CU traits. Since the three groups did not significantly differ in peak respiratory frequency, we may conclude that the observed differences in RSA level cannot be attributed to differences in respiratory frequency. This suggests that the high CU group was characterized by an abnormally low cardiac vagal tone. Although reduced RSA has been repeatedly observed in children or adolescents with DBD (Beauchaine
2001; Beauchaine et al.
2001,
2007,
2008; de Wied et al.
2009; Mezzacappa et al.
1997), a specific relationship with CU traits has not earlier been reported. It is important to mention in this connection that RSA scores were found to be inversely related to CU scores within the DBD group (
r = −40,
p = 0.026). Similar to reduced HR reactivity, reduced resting RSA in boys with CU traits may be an expression of structural or functional changes in brain circuits involving the ACC.
Limitations and Strengths
Several limitations of this study should be noted. First, the DBD sample was relatively small which makes it difficult to demonstrate significant differences between subgroups of DBD adolescents due to power limitations. Second, because the current study included only male adolescents, the findings require replication with female samples before they can be generalized to female adolescents with DBD. Third, because a majority of the DBD group showed comorbid ADHD, we cannot tell whether the results are exemplary for adolescents with pure DBD, or comorbid DBD/ADHD. ADHD is related to DBD (Matthys and Lochman
2010) and therefore redundant as adjustment variable. Further research is needed to examine the independent effects of DBD and ADHD upon empathic behavior.
Strengths of our study can be seen in the inclusion of a well-defined sample of DBD adolescents, with high CU respondents (i.e., those with CU scores well above average) showing significantly higher levels of aggressive/rule-breaking behavior than low CU respondents. A further strength is the inclusion of positive and negative target emotions. Our results confirm that the nature of target emotions affects empathy-related responding in DBD adolescents. The findings encourage further research on empathy problems associated with DBD in relation to a broader range of target emotions, especially fear and anxiety.
Clinical Implications
If replicated, the findings may have clinical significance. In clinical practice it is important to discriminate conduct disordered children with CU traits from those without such traits because they may require different approaches to intervention. Our findings demonstrate distinct deficits in the autonomic (not verbal or facial) expression of empathic sadness across DBD subgroups, suggesting that the mechanisms underlying empathy problems may be different for those with high versus low CU traits. The multidimensional study of empathy may advance our understanding about the mechanisms underlying empathy problems in subgroups of DBD children and adolescents. If laboratory markers of empathy can be developed that distinguish between subtypes of DBD individuals (as autonomic indexes of empathy), such instruments could be quite useful as part of an assessment battery.
Broadening our understanding about the processes underlying deficits in the development of empathy proposed for DBD children and adolescents is likely to inform treatment options. Empathy training is often part of prevention and intervention programs for antisocial youth, as the EQUIP program (Gibbs
2003). Knowledge about the nature of empathy problems associated with DBD may have important implications for developing more individualized training programs aimed to strengthen empathic skills in DBD children and adolescents.
In sum, the data confirm that CU traits designate a subgroup of DBD adolescents who exhibit particularly high levels of aggression and delinquency. The data demonstrate that DBD adolescents with high CU traits show consistent impairments in empathic sadness across different response systems. Moreover, relative to those with low CU traits, DBD adolescents with high CU traits show reduced HR change from baseline while witnessing another person in distress. The data also demonstrate that DBD adolescents with high CU traits show subnormal tonic parasympathetic activation of the cardiac system (reflected by reduced RSA). Our findings support the notion that CU traits identify a distinct subgroup of DBD individuals, which is in line with the suggestion to include CU traits as a qualifier for CD in the DSM-V (e.g., Frick and Moffit
2010).