Gray matter changes in right superior temporal gyrus in criminal psychopaths. Evidence from voxel-based morphometry
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)
The roles of orbital frontal cortex in the modulation of antisocial behavior
Brain and Cognition
(2004)- et al.
Quantitative frontal and temporal structural MRI studies in personality-disordered offenders and control subjects. Psychiatry Research
Neuroimaging
(2002) - et al.
A voxel-based morphometric study of ageing in 465 normal adult human brains
Neuroimage
(2001) - et al.
Temporal lobe abnormalities in semantic processing by criminal psychopaths as revealed by functional magnetic resonance imaging. Psychiatry Research
Neuroimaging
(2004) - et al.
Reduced temporal lobe volume in early onset conduct disorder. Psychiatry Research
Neuroimaging
(2004) - et al.
A volumetric MRI study of the hippocampus in type 1 and 2 alcoholism
Behavioural Brain Research
(2000) - et al.
Psychopathy and the posterior hippocampus
Behavioural Brain Research
(2001) - et al.
Prefrontal volumes in habitually violent subjects with antisocial personality disorder and type 2 alcoholism. Psychiatry Research
Neuroimaging
(2002) - et al.
Functional imaging of face and hand imitation: towards a motor theory of empathy
Neuroimage
(2004) - et al.
Abnormalities in emotion processing within cortical and subcortical regions in criminal psychopaths: evidence from a functional magnetic resonance imaging study using pictures with emotional content
Biological Psychiatry
(2003)