Abstract
Background
Contemporary theories and evidence implicate defective emotion regulation in violent behaviour. The two psychiatric illnesses most implicated in violence are schizophrenia and antisocial personality disorder (APD). This study examined behavioural and brain abnormalities in violent men with schizophrenia or APD during anticipatory fear.
Method
Fifty-three men [14 non-violent healthy controls, 13 with schizophrenia and a history of serious violence (VSZ), 13 with schizophrenia without a history of violence (SZ), 13 with APD and a history of serious violence] underwent blood-oxygenation-level-dependent fMRI during an experiment involving repeated presentations of ‘safe’ and ‘threat of electric shock’ conditions and provided ratings of shock anticipation and fear. Schizophrenia patients did not have co-morbid APD.
Introduction
Violent behaviour is associated with certain mental disorders, most markedly schizophrenia (Arseneault et al., 2000) and antisocial personality disorder (APD) (Hodgins, 1992). Although positive symptoms may drive inpatient violence, several other factors contribute on their own or in interaction with symptoms to persistent violence in the community shown by schizophrenia patients (Krakowski, 2005).
Dysfunction within a neural circuit implicated in emotion regulation is considered to constitute the neural substrates of violence (Davidson et al., 2000). This circuit includes several regions of the prefrontal cortex, amygdala, hippocampus, hypothalamus, anterior cingulate (AC), striatum and other interconnected structures (Davidson et al., 2000). Behaviourally, schizophrenia patients with a history of violent behaviour show a better ability to identify facial emotional expressions but a poorer ability to discriminate between intensity of emotions compared to non-violent schizophrenia patients (Silver et al., 2005). Schizophrenia patients with high psychopathy scores show impaired recognition of sadness at low intensity compared to those with low psychopathy scores (Fullam and Dolan, 2006). Despite the vast literature showing cortico-limbic abnormalities during processing of affective information (e.g. Gur et al., 2002 and Williams et al., 2004), previous studies have not examined functional brain abnormalities using an affective processing paradigm in association with persistent violent behaviour in schizophrenia.
There is reliable evidence of impaired ability to anticipate punishment, reduced psychophysiological responsiveness to threatening events, and reduced experience of aversive states in individuals with high psychopathic traits who form part of a wider group of people with APD (review, Herba et al., 2004). Studies of psychopathic/APD individuals suggest that altered functions mainly of regions located within the frontal and temporal lobes, that are implicated in response inhibition, modulation of aggressive or submissive behaviour, recognition of expressions of fear and anger, and fear conditioning, are involved in mediation and expression of psychopathy and antisocial behaviour (reviews, Herpertz and Sass, 2000, Dolan, 2002, Herba et al., 2004 and Kumari and Taylor, In press). Event-related potentials and imaging studies of psychopathic individuals by Kiehl and colleagues have shown paralimbic dysfunction and associated behavioural abnormalities in psychopathy (review, Kiehl, 2006).
In this study we examined neural dysfunctions, measured with functional magnetic resonance imaging (fMRI), associated with a history of serious physical violence during an anticipatory fear paradigm (Chua et al., 1999 and Kumari et al., 2007) in schizophrenia. We also studied a group with APD and a history of similar level of violence to that in patients with schizophrenia to elucidate common and distinct brain correlates of violence in these two disorders. We hypothesized, albeit with limited confidence given the lack of relevant imaging data in schizophrenia, that both violent groups would show altered fronto-temporal activity. We also predicted that our experimental manipulation involving an aversive procedure would be the least effective in violent APD individuals.
. Conclusions
This study demonstrated stronger aversive conditioning in men with schizophrenia and a history of violence than in men with APD and a similar violence history, with intermediate range for non-violent individuals (SZ men without a history of violence, healthy men), and aberrant activity modulation when exposed to threat cues over a sustained period in regions within the default node network in violent (VSZ, APD) compared to non-violent (SZ, HC) individuals, and opposite patterns of alternations in thalamic-striatal activity in VSZ (enhanced) and APD individuals (reduced). The common abnormality in the default mode regions in VSZ and APD most likely arises from dissimilar behavioural mechanisms, related to differences in the strength of aversive conditioning and processing of sustained threat cues, underscoring the need for differential strategies to manage violent behaviour in these two disorders.
Role of the funding source
The sponsors had no role in study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the paper for publication.
Contributors
Pamela Taylor and Veena Kumari contributed to funding acquisition. Veena Kumari, Mrigendra Das, Steven Williams and Christopher Andrew contributed to the development of experimental paradigm and other imaging aspects. Pamela Taylor and Mrigendra Das contributed to clinical aspects. Mrigendra Das, Ian Barkataki and Alexander Sumich contributed to imaging and behavioural data acquisition. Veena Kumari, with advice from Dominic ffytche, analysed the data and prepared the first draft. All authors contributed to the final version.
Conflict of interest
The authors declare no conflict of interest.