Elsevier

NeuroImage

Volume 37, Issue 1, 1 August 2007, Pages 335-342
NeuroImage

A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy

https://doi.org/10.1016/j.neuroimage.2007.04.043Get rights and content

Abstract

The goal of this study was to determine whether brain regions implicated in emotion processing show structural alterations in adolescents with conduct disorder (CD). Using an optimized voxel-based morphometry protocol, we compared grey matter volume in 12 patients with CD and 12 age-, sex-, and intelligence-matched control subjects. Grey matter volume in bilateral anterior insular cortex and the left amygdala was significantly reduced in CD patients compared to healthy control subjects. The insular grey matter abnormalities could be attributed to aggressive behaviour. Moreover, bilateral anterior insular grey matter volume in CD patients correlated significantly with empathy scores. These novel findings point at a joint neuroanatomical substrate underpinning aggressive behaviour and impaired capacity of empathy and suggest a critical role for the anterior insula in regulating social behaviour.

Introduction

The problem of juvenile delinquency and violence in modern societies has stimulated the search for factors that may predispose to aggressive behaviour. Despite the undisputable importance of socio-economic and political factors, the understanding of pathological aggression should benefit from identifying its biological basis (Davidson et al., 2000).

The propensity for aggressive and violent behaviour has been proposed to indicate a profound disturbance in an appropriate empathic response to the suffering of another (Blair, 2005, Frick et al., 1994, Miller and Eisenberg, 1988, Pardini et al., 2003, Soderstrom, 2003). Such lack of empathy could result from a dysfunction of neural circuits involved in recognizing emotional expressions that indicate distress in other individuals (Blair, 2001, Blair, 2005, Davidson et al., 2000). Functional neuroimaging studies of emotion processing in aggressive and violent individuals indeed support this view by demonstrating functional deficits in brain regions involved in emotion recognition, most notably the amygdala (Birbaumer et al., 2005, Kiehl et al., 2001, Sterzer et al., 2005, Veit et al., 2002). In addition to relying on emotion recognition, empathy may also involve brain structures which in general serve the representation of emotional and bodily states of arousal (Craig, 2002, Critchley, 2005, Damasio, 2003). Accordingly, recent functional neuroimaging studies investigating the mechanisms of empathy for pain (Jackson et al., 2005, Jackson et al., 2006, Singer et al., 2004, Singer et al., 2006) and disgust (Wicker et al., 2003) or imitation of emotional facial expression (Carr et al., 2003) support the notion of a central involvement of anterior insular cortex in empathy (for overviews, see de Vignemont and Singer, 2006, Decety and Lamm, 2006, Gallese et al., 2004).

In addition to deficient empathy, it has been proposed that aggressive and antisocial behaviour may arise from functional deficits in brain regions involved in the regulation of emotional behaviour, most importantly orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC) (Adolphs, 2003, Davidson et al., 2000). OFC is thought to constrain affective impulses through its connections with other prefrontal regions and the amygdala, as suggested by evidence from the study of patients with OFC lesions (Anderson et al., 1999) as well as structural (Raine et al., 2000) and functional neuroimaging (Kiehl et al., 2001, Raine et al., 1998) in antisocial and psychopathic individuals. ACC plays an important role in the regulation of cognitive and emotional processes (Bush et al., 2000), and abnormal function in this region has been observed in patients with conduct disorder (Sterzer et al., 2005), antisocial personality disorder (Veit et al., 2002), and in criminal psychopaths (Kiehl et al., 2001). While in normal individuals these brain regions act to constrain the expression of affect, deficits in this circuit are hypothesized to increase a person's inclination towards vulnerability to aggressive behaviour (Davidson et al., 2000).

Here, we asked whether aggressive behaviour might be associated with structural deficits in brain regions implicated in emotion recognition, empathy, and emotion regulation. We used structural magnetic resonance (MR) imaging in conjunction with voxel-based morphometry (VBM) to examine grey matter abnormalities in adolescents with conduct disorder (CD). CD is characterized by repetitive and chronic aggressive and antisocial behaviour in which the basic rights of others or major age-appropriate norms or rules of society are violated and that has a variety of implications such as school refusal, social communication problems, and legal involvement (American Psychiatric Association, 1994). CD is often associated with other psychiatric diagnoses, most prominently attention-deficit hyperactivity disorder (ADHD) and anxiety disorders (Loeber et al., 2000). The participants were therefore carefully assessed with respect to symptoms of such co-morbidities, enabling us to test whether any volumetric differences between CD patients and normal control subjects could be attributed to aggressive behaviour. Finally, reduced empathy may be an important factor predisposing to aggressive behaviour, as outlined above. We therefore determined empathy levels psychometrically and probed their association with regional grey matter volume in CD patients.

Section snippets

Subjects and behavioural measures

Twelve male adolescents with CD recruited from the specialized ‘aggression clinics’ of the Department of Child and Adolescent Psychiatry and twelve age- and intelligence-matched male control subjects recruited from secondary schools volunteered for the experiment. All participants were white Caucasian and were born and raised in Germany. None of the participants had a history of traumatic brain damage or other neurological diseases. None of the control subjects had any history of psychiatric

Demographic and behavioural results

Patients and control subjects did not differ significantly in age, intelligence, or parental socio-economic state (Table 1). As expected, CBCL scores for aggressive behaviour and delinquent behaviour, i.e., the diagnosis-defining features in CD, were significantly higher in the patient group (Table 1). Scores for social withdrawal, anxiety/derepression, and attention problems also showed significant group differences. Psychometric testing using the IVE questionnaire revealed significantly lower

Discussion

To our knowledge, this is the first study to show structural brain abnormalities associated with aggressive behaviour as early as in adolescence. Reduced grey matter volume in CD patients compared to controls was detected in the left amygdala and the anterior insula bilaterally. Importantly, the group differences in bilateral anterior insula cortex could be related to aggressive behaviour. Moreover, empathy levels in the patient group correlated with anterior insular grey matter volume but not

Conclusion

We demonstrate a morphological neural correlate of pathological aggressive behaviour as early as in adolescence. Moreover, our results extend the relation between empathy and the brain both to the structural neural and the pathological behavioural level and hence provide a putative neurobiological substrate for the long-standing proposal that a lack of empathy might predispose towards violent social behaviour (Blair, 2005).

Acknowledgments

This work was supported by the Volkswagen Foundation (PS and AK) and by the German Research Society (PS).

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