Research report
Volumetric structural brain abnormalities in men with schizophrenia or antisocial personality disorder

https://doi.org/10.1016/j.bbr.2006.01.009Get rights and content

Abstract

Brain abnormalities are found in association with antisocial personality disorder and schizophrenia, the two mental disorders most implicated in violent behaviour. Structural magnetic resonance imaging was used to investigate the whole brain, cerebellum, temporal lobe, lateral ventricles, caudate nucleus, putamen, thalamus, hippocampus, amygdala and the prefrontal, pre-motor, sensorimotor, occipito-parietal regions in 13 men with antisocial personality disorder, 13 men with schizophrenia and a history of violence, 15 men with schizophrenia without violent history and 15 healthy non-violent men. Compared to controls, the antisocial personality disorder group displayed reductions in whole brain volume and temporal lobe as well as increases in putamen volume. Both schizophrenia groups regardless of violence history exhibited increased lateral ventricle volume, while the schizophrenia group with violent history showed further abnormalities including reduced whole brain and hippocampal volumes and increased putamen size. The findings suggest that individuals with antisocial personality disorder as well as those with schizophrenia and a history of violence have common neural abnormalities, but also show neuro-anatomical differences. The processes by which they came to apparently common ground may, however, differ. The finding of temporal lobe reductions prevalent among those with antisocial personality disorder and hippocampal reduction in the violent men with schizophrenia contributes support for the importance of this region in mediating violent behaviour.

Introduction

Violent behaviour is disproportionately over-represented in individuals with certain mental disorders compared with the general population [15]. Schizophrenia and antisocial personality disorder (APD) are the disorders most implicated in violence [15], [47]. Existing psycho-physiological and neuropsychological studies have demonstrated similar impairments in APD and the related dimensional concept of psychopathy, as well as in schizophrenia [4], [22], [36]. These overlapping deficits include impairment in the ability to correctly interpret and recognise facial affect [4], [5], [22] and decreased executive functioning capacity, when compared to healthy control subjects [12], [36].

Although the role of biological factors in relation to mental disorder remains uncertain, these functional impairments have been used as evidence of neural pathology, which may be directly or indirectly involved in the expression of violent behaviour. Animal studies and theoretical accounts suggest that aggression is elicited by neurological trauma or lesions to the prefrontal cortex (PFC), temporal lobes and hypothalamus [49], [41]. These areas are associated with higher intellectual functioning and goal-directed behaviour but are also implicated in mediating emotion and inhibitory mechanisms [8]. Although many studies refer to ‘aggression’; a catchall category likely to refer to attitude or angry affect as well as physical acts, the current study is concerned with actual physical violence, independently recognised as serious in all cases.

The advent of neuroimaging techniques such as magnetic resonance imaging (MRI) has helped investigators to uncover structural neural characteristics and abnormalities occurring in people who have a propensity for violence. Reviews of structural MRI investigations among people with schizophrenia [40], [52] have consistently concluded that schizophrenia appears to be associated with reduction in whole brain size, cortical grey matter, thalamus, temporal and frontal lobe volume, as well as increased cerebral ventricle and basal ganglia volume. Studies specifically examining individuals with schizophrenia and a history of violence have reported reductions in whole brain and hippocampal volume [7], temporal lobe volume reductions [50] and frontal lobe white matter abnormalities [24].

There are fewer neuroimaging studies of people with APD. One recent review of APD research [8] noted consistent findings of reductions in the temporal lobe (particularly the amygdala) and frontal lobes. A structural MRI study [13] that examined antisocial and borderline personality disordered sample reported reductions in temporal lobe volume when compared to healthy controls, but did not find any significant frontal lobe volume decrease. Other investigations of personality-disordered samples (including APD) have reported ventricular enlargement [51] and reductions in prefrontal cortex grey matter [37] when compared to healthy individuals. Additionally, a study of psychopathy in APD conducted by Laakso et al. [29] demonstrated a strong negative correlation between antisocial traits and posterior hippocampus volume, where higher trait scores were linked to lower volume. Such reductions in temporal lobe size (in addition to the hippocampus and amygdala) are linked to impaired emotional processing in APD [28], increases in impulsivity and predisposition towards violent behaviour [9]. These regions have also been implicated in schizophrenia populations, where similar observations of fronto-temporal abnormalities have been associated with hallucinations and delusions, and the onset of psychosis [30], [45]. Impaired emotional processing is a problem also for many people with schizophrenia, although delusions are the features that have been most consistently related to violent acts [47].

Previous structural MRI investigations among people with mental disorder who have been violent have grouped together diverse psychiatric conditions under the common factor of ‘violence’, or have included subjects with co-morbid mental disorders [8]. With these limitations in mind, in the current study we sought, using structural MRI methods, to compare neural differences in groups of men diagnosed with APD or with schizophrenia, in the latter case with and without history of violence, as well as healthy controls. The study focussed on men due to the relative scarcity of women in forensic secure settings that would fulfil the study's inclusion criteria, as well as the fact that a purely male sample would eliminate confounding factors that may be related to sex.

Based on the existing literature, it was hypothesised that: (i) the APD group would have smaller temporal lobes, pre-frontal cortex and constituent limbic system components (amygdala and hippocampus) compared to controls, (ii) both violent and non-violent groups with schizophrenia would display a reduction in whole brain volume as well as in limbic structures and the thalamus but increased volumes of lateral ventricles, caudate nucleus and putamen compared to controls, and (iii) the violent men with schizophrenia would show more extensive abnormalities in structural volumes than their non-violent peers, due to the combination of violence and pre-existing mental illness.

Section snippets

Subjects

The violent men with mental disorder were recruited from one high security hospital (Broadmoor) and one medium security hospital unit (Denis Hill Unit, Bethlem Royal Hospital). The non-violent men with schizophrenia were recruited from open psychiatric settings in the South London and Maudsley Trust, London, and the healthy control men were recruited by advertisement and employment agencies local to the latter Trust. An attempt was made to recruit violent men without either personality disorder

Demographic and clinical data

Means and standard deviations and ANOVA comparisons for demographic and clinical variables are provided in Table 1. Chi-square analysis of ethnicity (χ2 = 13.932, p = 0.53), education (χ2 = 9.76, p = 0.37) or socio-economic status (χ2 = 28.35, p = 0.06) did not reveal any significant group differences. The VS and APD groups did not statistically differ in the subtypes of violent crimes they committed (χ2 = 0.397, p = 0.98). On other demographic and clinical measures, the four groups were similar but they did

Discussion

This study investigated structural abnormalities in brain regions specifically implicated as anomalous in men with schizophrenia and APD that are violence prone. The findings revealed differential as well as shared abnormalities in the two violent groups and the two schizophrenia groups, in addition to revealing certain features specific to individual groups.

Specifically, compared to controls, the APD group displayed reductions in whole brain volume, temporal lobe and increases in putamen

Acknowledgments

We express our appreciation to the staff of Broadmoor Special Hospital and the Denis Hill Unit of the Royal Bethlem Hospital for assistance with this study. We would also like to thank Prof. Sheilagh Hodgins for her comments on an earlier draft of this paper. This study was funded by grants from The Zito Trust and the Community Fund, UK, and the Stanley Medical Research Institute, USA. Veena Kumari holds a Wellcome Trust Senior Research Fellowship in Basic Biomedical Science.

References (51)

  • K.A. Kiehl et al.

    Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging

    Biol Psychiat

    (2001)
  • M. Laakso et al.

    Psychopathy and the posterior hippocampus

    Behav Brain Res

    (2001)
  • I.K. Lyoo et al.

    A brain MRI study in subjects with borderline personality disorder

    J Affect Disord

    (1998)
  • T. Sharma et al.

    Lack of normal pattern of cerebral asymmetry in familial schizophrenic patients and their relatives—the Maudsley family study

    Schizophr Res

    (1999)
  • M. Shenton et al.

    A review of MRI findings in schizophrenia

    Schizophr Res

    (2001)
  • A. Siegel et al.

    Neuropharmacology of brain stimulation evoked aggression

    Neurosci Biobehav Rev

    (1999)
  • H. Soderstrom et al.

    Reduced fronto-temporal perfusion in psychopathic personality

    Psychiat Res

    (2002)
  • M. Wong et al.

    Positron emission tomography in male violent offenders with schizophrenia

    Psychiat Res

    (1997)
  • R.M. Bilder et al.

    Absence of regional hemispheric volume asymmetries in first-episode schizophrenia

    Am J Psychol

    (1994)
  • R. Blair

    Neurobiological basis of psychopathy

    Br J Psychiat

    (2003)
  • L. Chesterman et al.

    Multiple measures of cerebral state in dangerous mentally disordered inpatients

    Crim Behav Mental Health

    (1994)
  • M. Das et al.

    Neuroimaging violence in the mentally ill: what can it tell us?

    Hosp Med

    (2002)
  • R.J. Davidson et al.

    Dysfunction in the neural circuitry of emotion regulation—a possible prelude to violence

    Science

    (2000)
  • S. DeArmond et al.

    Structure of the human brain: a photographic atlas

    (1989)
  • W. Dinn et al.

    Neurocognitive function in antisocial personality disorder

    Psychiat Res

    (2000)
  • Cited by (0)

    View full text