Gray matter changes in right superior temporal gyrus in criminal psychopaths. Evidence from voxel-based morphometry

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Abstract

“Psychopathy” according to the PCL-R describes a specific subgroup of antisocial personality disorder with a high risk for criminal relapses. Lesion and imaging studies point towards frontal or temporal brain regions connected with disturbed social behavior, antisocial personality disorder (APD) and psychopathy. Morphologically, some studies described a reduced prefrontal brain volume, whereas others reported on temporal lobe atrophy. To further investigate whether participants with psychopathy according to the Psychopathy Checklist — Revised Version (PCL-R) show abnormalities in brain structure, we used voxel-based morphometry (VBM) to investigate region-specific changes in gray matter in 17 forensic male inpatients with high PCL-R scores (PCL-R > 28) and 17 male control subjects with low PCL-R scores (PCL < 10). We found significant gray matter reductions in frontal and temporal brain regions in psychopaths compared with controls. In particular, we found a highly significant volume loss in the right superior temporal gyrus. This is the first study to show that psychopathy is associated with a decrease in gray matter in both frontal and temporal brain regions, in particular in the right superior temporal gyrus, supporting the hypothesis that a disturbed frontotemporal network is critically involved in the pathogenesis of psychopathy.

Introduction

A growing body of research is examining the nature an biological basis of social functioning and behavior. In criminal psychopathy, a specific subgroup of antisocial personality disorder, emotional detachment and disturbed interpersonal relationship may lead to social dysfunction and criminal behavior (Ratiu et al., 2004, Blair, 2004). Thus, research on the neurobiology of psychopathy may provide a context to study the neural underpinnings of violent and antisocial behavior, deficient emotion processing, and the neurology of decision-making (Laakso et al., 2001).

Psychopathy defined by Hare's Psychopathy Checklist — Revised Version (Hare, 1991) describes a specific subgroup of antisocial personality disorder (APD) according to DSM-IV or dissocial personality disorder according to ICD-10. Hare (1991) characterizes, psychopathy as comprising two correlated factors: emotional detachment (Factor 1) and antisocial behavior (Factor 2). Regarding the two-factor model, emotional detachment (Factor 1) emphasizes the abnormal emotional responsiveness as a key feature of psychopathy and distinguishes between psychopathy and other antisocial personality disorders. Thus, APD is only weakly associated with PCL-R score. More than 50% of the American prison population consists of APD, whereas less than 30% of the prison population fulfill the criteria for psychopathy (Hare et al., 2000). The PCL-R has been successfully introduced as an instrument for risk assessment (Hare, 1991, Hare et al., 2000). Recent investigations evaluate concepts using three- or four- factor models (Cooke and Mitchie, 2001). Thus, the concept of psychopathy has emerged as important, especially in forensic psychiatry.

Clinically, psychopaths have been described as selfish, dominant, manipulative and superficial, showing a lack of responsibility within relationships and an inability to form long-lasting bonds. Psychopaths are supposed to be impulsive, showing sensation seeking behavior and having low frustration tolerance. Within the affective domain, psychopaths are described as fearless, shallow and callous. They are described as showing emotional detachment, unable to experience deeper feelings of love. Empathy and remorse are found to be lacking, and at the same time psychopaths are indifferent to the feelings of others. As a function of their deficient emotional reactivity, criminal psychopaths have been found to be unable to learn from negative experiences like punishment. Thus, their forensic prognosis is bad (Hare, 1991, Hare et al., 2000).

Since the famous case of Phineas Gage, lesion studies linked prefrontal, in particular, ventromedial and orbitofrontal cortical damage, to impairment in social behavior and decision-making. Because prefrontal brain lesions may result in a pseudopsychopathic syndrome, so-called “acquired psychopathy” (Barrash et al., 2000, Blair and Cipolotti, 2000, Tranel, 1994, Meyers et al., 1992, Müller et al., 2003b), prefrontal brain structure and function have been hypothesized to be crucially involved in social behavior. In order to verify this hypothesis, Raine et al. investigated 21 persons with antisocial personality disorder (APD) without brain trauma. They found an 11.0% reduction in prefrontal gray matter volume in the absence of ostensible brain lesions and a reduced autonomic activity during stressor exposure in the APD group (Raine et al., 2000). Yang et al. evaluated the influence of social success on prefrontal brain volume in psychopaths and reported a 22.3% prefrontal gray matter reduction in unsuccessful (caught) psychopaths, whereas successful (uncaught) psychopaths showed normal prefrontal volumes (Yang et al., 2005a). Furthermore, a prefrontal white matter increase and a reduction in the prefrontal gray/white matter ration were found to be associated with pathological lying (Yang et al., 2005b), one of the PCL-R items.

Focusing on the impact of the prefrontal cortex in psychopathy as well, Laakso et al. investigated the patterns of prefrontal volume loss and their specifity for antisocial behavior and the correlation between prefrontal volume and the degree of psychopathy (Laakso et al., 2002). They found significantly smaller left dorsolateral, medial frontal and orbitofrontal cortices in persons with antisocial personality disorders. However, after they controlled for differences in education and duration of alcoholism, these differences in volume disappeared. For the dorsolateral and orbitofrontal cortices, only the duration of alcoholism was significantly associated with the observed volume deficit, and for the medial frontal cortex it was educational level that correlated best with the changes seen. Thus, the observed volume deficits were related more closely to alcoholism or differences in education than to the diagnosis of antisocial personality disorder per se (Laakso et al., 2002). This finding raised the question of whether alcohol consumption should be seen as an independent covariate or as a major feature of APD. The impact of prefrontal volume loss in psychopathy was also rejected by Dolan et al. (Dolan et al., 2002) who investigated incarcerated impulsive–aggressive personality-disordered (PD) offenders. Despite impaired executive function, frontal lobe volume was not reduced in PD (Dolan et al., 2002). Interestingly, Dolan et al. found 20% smaller temporal lobe volumes in PD in comparison to control subjects (Dolan et al., 2002). This finding was confirmed by Barkataki et al. (2006), who compared APD to schizophrenia in males and found a volume reduction in the temporal lobe in APD.

Furthermore, hippocampal atrophy has been linked to APD in violent forensic patients, in late-onset type 1 alcoholics and early-onset type 2 alcoholics (Laakso et al., 2000), and in unsuccessful, caught psychopaths compared with successful uncaught community psychopaths (Raine et al., 2004). The hypothesis that frontotemporal brain regions, as a functional network, are critically involved in the pathogenesis of psychopathy is supported by recent functional magnetic resonance imaging (fMRI) data (Kiehl et al., 2004, Müller et al., 2003a, Müller et al., 2003b, Birbaumer et al., 2005) and by electrophysiological data (Kiehl et al., 2006) pointing to frontotemporal dysfunction in psychopathy.

Finally, the corpus callosum has been focused on, since interhemispheric processing and callosal functioning are believed to be disturbed in (psychopathic) antisocial individuals. Psychopaths showed a 22.6% increase in callosal white matter volume, a 6.9% increase in callosal length, a 15.3% reduction in callosal thickness, and an increased functional interhemispheric connectivity (Raine et al., 2003).

In spite of growing evidence of frontotemporal abnormalities in psychopathy, results are still heterogeneous, stressing morphological abnormalities either in frontal or temporal brain regions. Regarding structural imaging studies, this might depend on heterogeneous inclusion criteria as well as on heterogeneous evaluation methods focusing on different regions of interest that had been defined before the investigation.

In order to perform a whole brain analysis that would allow us to take into account both frontal and temporal regions, we used voxel-based morphometry looking for subtle, region-specific differences in gray matter between controls and patients fulfilling the diagnostic criteria for psychopathy according to Hare (Hare et al., 1991,2000). In addition, we performed region of interest analyses with respect to the hypothesis that the frontotemporal brain network is critically involved in the pathogenesis of psychopathy. Finally, we performed correlational analyses with the individual duration of alcohol and drug dependency, time of education and duration of detention as predictors.

Section snippets

Study population (Table 1)

17 patients (n = 17; mean age = 33.00 years (22–44 years; S.D. = 5.81) and 17 healthy male volunteers (n = 17; mean age = 30.59 years (23–42 years; S.D. =5.92) participated in this study. There was no significant difference in age between the two groups (P > 0.05; n.s.). Both groups consisted of male participants only. According to the inclusion criteria, forensic inpatients fulfilled the diagnostic criteria for psychopathy with or without a history of substance dependency. Participants with other

Brain structure

Conventional MR-imaging was normal in all patients and controls.

Cohort analysis

Voxel-based morphometry (VBM) revealed that psychopathy shows a highly significant (P < 0.05 corr.) association with a decrease in gray matter volume in the right superior temporal gyrus (x = 42, y = 15, z =  32). Region of interest analyses revealed decreased gray matter in the left superior temporal gyrus (x =  36, y = 18, z =  32), the right middle frontal gyrus (x = 35, y = 18, z = 53), and the right (middle) cingulate gyrus (x = 5, y =  13, z = 34)

Discussion

In spite of growing interest in the neurobiology of psychopathy, there are only a few studies investigating brain structure in psychopaths. Results are still heterogeneous (Pridmore et al., 2005). Various studies linked psychopathic behavior to abnormal frontal and/or temporal lobe structure and function. A prefrontal volume deficit in psychopathy was found by different research groups (Raine et al., 2000, Blair, 2004, Yang et al., 2005a), while other authors failed to confirm these data (Dolan

References (45)

  • J. Narumoto et al.

    Attention to emotion modulates fMRI activity in human right superior temporal sulcus

    Cognitive Brain Research

    (2001)
  • S.M. Platek et al.

    Where am I? The neurological correlates of self and other

    Cognitive Brain Research

    (2004)
  • A. Raine et al.

    Hippocampal structural asymmetry in unsuccessful psychopaths

    Biological Psychiatry

    (2004)
  • H. Soderstrom et al.

    Reduced frontotemporal perfusion in psychopathic personality. Psychiatry Research

    Neuroimaging

    (2002)
  • B. Völlm et al.

    Neural correlates of theory of Mind and empathy: a functional magnetic resonance imaging study in a nonverbal task

    Neuroimage

    (2006)
  • F.G. Woermann et al.

    Voxel-by-voxel comparison of automatically segmented cerebral gray matter—a rater-independent comparison of structural MRI in patients with epilepsy

    Neuroimage

    (1999)
  • Y. Yang et al.

    Volume reduction in prefrontal gray matter in unsuccessful criminal psychopaths

    Biological Psychiatry

    (2005)
  • J. Ashburner et al.

    Voxel-based morphometry—the methods

    Neuroimage

    (2001)
  • J. Ashburner et al.

    Image registration using a symmetric prior — in three dimensions

    Human Brain Mapping

    (2000)
  • J. Barkataki et al.

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

    Behavioural Brain Research

    (2006)
  • J. Barrash et al.

    Acquired personality disturbances associated with bilateral damage to the ventromedial prefrontal region

    Developmental Neuropsychology

    (2000)
  • A.J. Bartsch et al.

    Manifestations of early brain recovery associated with abstinence from alcoholism

    Brain

    (2007)
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