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Altered Connections on the Road to Psychopathy

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Altered Connections on the Road to Psychopathy Molecular Psychiatry (2009) 14, 946–953 & 2009 Nature Publishing Group All rights reserved 1359-4184/09 $32.00 www.nature.com/mp ORIGINAL ARTICLE Altered connections on the road to psychopathy MC Craig1,2, M Catani1,2, Q Deeley1, R Latham1, E Daly1, R Kanaan3, M Picchioni3, PK McGuire3, T Fahy4 and DGM Murphy1 1Section of Brain Maturation, Institute of Psychiatry, De Crespigny Park, London, UK; 2Natbrainlab, Institute of Psychiatry, De Crespigny Park, London, UK; 3Section of Neuroimaging, Institute of Psychiatry, De Crespigny Park, London, UK and 4Department of Forensic Mental Health Science, Institute of Psychiatry, De Crespigny Park, London, UK Psychopathy is strongly associated with serious criminal behaviour (for example, rape and murder) and recidivism. However, the biological basis of psychopathy remains poorly under- stood. Earlier studies suggested that dysfunction of the amygdala and/or orbitofrontal cortex (OFC) may underpin psychopathy. Nobody, however, has ever studied the white matter connections (such as the uncinate fasciculus (UF)) linking these structures in psychopaths. Therefore, we used in vivo diffusion tensor magnetic resonance imaging (DT-MRI) tracto- graphy to analyse the microstructural integrity of the UF in psychopaths (defined by a Psycho- pathy Checklist Revised (PCL-R) score of X25) with convictions that included attempted murder, manslaughter, multiple rape with strangulation and false imprisonment. We report significantly reduced fractional anisotropy (FA) (P < 0.003), an indirect measure of micro- structural integrity, in the UF of psychopaths compared with age- and IQ-matched controls. We also found, within psychopaths, a correlation between measures of antisocial behaviour and anatomical differences in the UF. To confirm that these findings were specific to the limbic amygdala–OFC network, we also studied two ‘non-limbic’ control tracts connecting the posterior visual and auditory areas to the amygdala and the OFC, and found no significant between-group differences. Lastly, to determine that our findings in UF could not be totally explained by non-specific confounds, we carried out a post hoc comparison with a psychiatric control group with a past history of drug abuse and institutionalization. Our findings remained significant. Taken together, these results suggest that abnormalities in a specific amygdala– OFC limbic network underpin the neurobiological basis of psychopathy. Molecular Psychiatry (2009) 14, 946–953; doi:10.1038/mp.2009.40; published online 9 June 2009 Keywords: psychopathy; limbic system; white matter connections; diffusion tensor imaging; tractography Introduction ‘acquired sociopathy’ after frontal lobe injury, the orbitofrontal cortex (OFC) and other regions of the Psychopathic personality disorder (psychopathy) is prefrontal cortex (PFC) have been considered impor- characterized by features of emotional detachment tant for personality and social behaviour.6 For exam- and antisocial traits,1 and is strongly associated with ple, OFC is crucial to successful reversal learning criminal behaviour and recidivism.2 It has been esti- (in which previously rewarded stimuli are associated mated, for example, that 15% of the prison popula- with punishment) and reversal learning is signifi- tion are psychopaths and they commit approximately cantly impaired in adult psychopaths7 and in young 50% more criminal offences than non-psychopathic people with psychopathic traits.8 It has also been criminals.3 reported that violent personality-disordered offenders The development of reliable and valid methods have reduced PFC grey matter volume9 and glucose for diagnosing psychopathy (for example, the Hare metabolism,10 and impaired OFC (and limbic) activa- Psychopathy Checklist Revised; PCL-R4) in conjunc- tion during aversive conditioning.11 In contrast, other tion with brain-imaging techniques is converging researchers have argued that amygdala dysfunction is towards the identification of neurobiological mecha- central to the affective deficits and impaired moral nisms that may underpin psychopathy. Since the socialization of psychopathy.12 This latter view is report of the case of Phineas Gage,5 who showed supported by evidence that psychopaths show per- formance deficits in tasks sensitive to amygdala Correspondence: Dr MC Craig, Psychological Medicine, Institute damage,13,14 and have significantly reduced amygdala of Psychiatry, PO50, 16 De Crespigny Park, Denmark Hill, London volume15 and decreased amygdala activation during SE5 8AF, UK. 16 E-mail: [email protected] verbal learning and decreased activity in brain Received 7 August 2008; revised 25 February 2009; accepted 13 regions modulated by amygdala during facial fear April 2009; published online 9 June 2009 processing.17 Altered connections on the road to psychopathy MC Craig et al 947 More recently, the dichotomy between researchers PCL-R scores (that is, X25). Sixteen patients initially postulating whether OFC or amygdala dysfunction is agreed to participate and nine were suitable for central to psychopathy18 has narrowed, and it has magnetic resonance imaging (MRI). Healthy controls been suggested instead that the social and emotional were recruited from the general population through deficits of psychopaths may reflect an interaction the Institute of Psychiatry, Kings College London, and between OFC and amygdala dysfunction.19,20 Analy- the absence of psychopathy was confirmed using sis of the functional and anatomical links between the Hare Psychopathy Checklist: Screening Version these structures offers the potential to move beyond (PCL-SV).26 theories of regional dysfunction towards a more Ethical approval was obtained from the Ethical coherent understanding of the possible brain net- Committee of the South London and Maudsley Trust works underlying psychopathy. However, to date, and Institute of Psychiatry, and St Georges Healthcare nobody has studied the white matter tracts linking Trust. After complete description of the study to the these brain regions. The OFC and the amygdala are patients, written informed consent was obtained. interconnected by fibres belonging to the uncinate fasciculus (UF), whose volume and integrity can be Neuroimaging and data analysis analysed in vivo using diffusion tensor magnetic Magnetic resonance imaging of the brain was carried resonance imaging (DT-MRI) tractography. This is a out on GE Signa 1.5 Tesla LX MRI system (General non-invasive neuroimaging technique that can be Electric, Milwaukee, WI, USA) at the Maudsley used to reconstruct three-dimensional trajectories of Hospital, London. white matter tracts within the living brain,21 and to probe the microstructural integrity of white matter in DT-MRI acquisition. Data were acquired with a wide range of neuropsychiatric conditions.22 40 mT mÀ1 gradients, using an acquisition sequence We therefore used in vivo DT-MRI to dissect and fully optimized for DT-MRI of white matter, providing measure the volume and the microstructural integrity isotropic resolution (2.5 Â 2.5 Â 2.5 mm) and coverage of the UF.21 For each hemisphere, we dissected the of the whole head. The acquisition was gated to the fibres of the UF and counted the number of stream- cardiac cycle using a peripheral gating device placed lines (SLs) as a surrogate of the tract volume. We also on the patients’ forefinger. After the correction for measured the mean fractional anisotropy (FA)— image distortions introduced by the application of the which is an indirect measure of white matter spatial diffusion encoding gradients, the diffusion tensor was organization and integrity.23 We compared the psy- determined in each voxel following the method of chopaths (that is, PCL-R score X2524) with age- and Basser et al.27 The operator (Michael C. Craig) carried IQ-matched controls. We recruited psychopaths from out all dissections blind to the diagnosis. Anatomical three specialist forensic inpatient units. All were consistency with classical descriptions of the tracts of repeat violent offenders with index offences that interest was confirmed by using neuroanatomy text included attempted murder, manslaughter, multiple books and tractography atlases. rape with strangulation and false imprisonment. Tract reconstructions. The trajectories of the UF, inferior longitudinal fasciculus (ILF) and inferior Methods fronto-occipital fasciculus (IFOF) were each recon- Patients structed using an approach that involved dissecting We studied 18 normal intelligence right-handed adult out two regions of interest (ROIs)28 (Figure 1). male volunteers: nine with high PCL-R scores (mean The ILF is a ventral associative bundle with long 28.4, range 25–34), aged 34±12 years, with full-scale and short fibres connecting the occipital and temporal IQ (FSIQ) 94±7, and nine healthy male controls aged lobes.3,28 The long fibres are medial to the short fibres 37±9 years, with FSIQ 91±6. All patients (that is, in and connect occipital visual areas to the amygdala both groups) were unmedicated and screened by and hippocampus. The first (temporal) ROI used to formal psychiatric semi-structured interview using dissect the ILF was defined around the white matter the ICD-10 research criteria,25 and a review of case of the anterior temporal lobe, usually on five axial notes was carried out to exclude any co-morbid slices. The second (occipital) ROI was defined around psychiatric illness or neurological/extra-cerebral dis- the white matter of the occipital lobe, usually on orders that might affect brain function.
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