Psychopathy as a disorder of the moral brain: Fronto-temporo-limbic grey matter reductions demonstrated by voxel-based morphometry

Major advances have been made in the understanding of the neurobiology of psychopathy in the past years, yet the distribution and extent of neuroanatomical abnormalities underlying the disorder are still poorly known. It is also unclear if different dimensions of the construct of psychopathy (e.g., emotional callousness, antisocial behavior) correspond to structural abnormalities in distinct regions of the brain. We tested the following hypotheses: (1) psychopathy is related to grey matter reductions in regions of the brain that underlie moral conduct and (2) the severity of psychopathy is related to the degree of structural abnormalities. Optimized voxel-based morphometry and the screening version of the Psychopathy Checklist (PCL: SV) were employed to investigate a matched sample of 15 community psychiatric patients with high PCL: SV scores, and 15 healthy normal volunteers. The analyses controlled for total grey matter, white matter and cerebrospinal fluid volumes. Grey matter reductions were observed in the frontopolar, orbitofrontal and anterior temporal cortices, superior temporal sulcus region, and insula of the patients. The degree of structural abnormalities was significantly related to the interpersonal/affective dimension of psychopathy. The pattern of grey matter reductions in patients with high psychopathy scores comprised a distributed fronto-temporal network which plays a critical role in moral sensibility and behavior.

[1]  R D Hare,et al.  Psychopathy and choice of immediate versus delayed punishment. , 1966, Journal of abnormal psychology.

[2]  Estibaliz Arce,et al.  Hippocampal structural asymmetry in unsuccessful psychopaths , 2004, Biological Psychiatry.

[3]  J. O'Doherty,et al.  Empathic neural responses are modulated by the perceived fairness of others , 2006, Nature.

[4]  J. Monahan,et al.  A Classification Tree Approach to the Development of Actuarial Violence Risk Assessment Tools , 2000, Law and human behavior.

[5]  Todd Lencz,et al.  Corpus callosum abnormalities in psychopathic antisocial individuals. , 2003, Archives of general psychiatry.

[6]  H. D. Critchley,et al.  Social and motivational functioning is not critically dependent on feedback of autonomic responses: neuropsychological evidence from patients with pure autonomic failure , 2004, Neuropsychologia.

[7]  R. Blair,et al.  Risky decisions and response reversal: is there evidence of orbitofrontal cortex dysfunction in psychopathic individuals? , 2002, Neuropsychologia.

[8]  J. Decety,et al.  The functional architecture of human empathy. , 2004, Behavioral and cognitive neuroscience reviews.

[9]  Olga V. Demler,et al.  Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. , 2005, Archives of general psychiatry.

[10]  J. Endicott,et al.  Global Assessment Scale (GAS) , 1996 .

[11]  Michael B. First,et al.  Handbook of Psychiatric Measures , 2000 .

[12]  H. Critchley,et al.  Neuroanatomical basis for first- and second-order representations of bodily states , 2001, Nature Neuroscience.

[13]  Roberto Colom,et al.  Fluid intelligence, working memory and executive functioning. , 2006, Psicothema.

[14]  J. Grafman,et al.  Opinion: the neural basis of human moral cognition. , 2005, Nature reviews. Neuroscience.

[15]  Neil Roberts,et al.  Quantitative frontal and temporal structural MRI studies in personality-disordered offenders and control subjects , 2002, Psychiatry Research: Neuroimaging.

[16]  P F Hall,et al.  Rethinking risk. , 1994, Canadian family physician Medecin de famille canadien.

[17]  A. Villringer,et al.  An fMRI study of simple ethical decision-making , 2003, Neuroreport.

[18]  J. Price.  Prefrontal Cortical Networks Related to Visceral Function and Mood , 1999, Annals of the New York Academy of Sciences.

[19]  Hanna Damasio,et al.  Does gender play a role in functional asymmetry of ventromedial prefrontal cortex? , 2005, Brain : a journal of neurology.

[20]  Robert D. Rogers.  The Functional Architecture of the Frontal Lobes: Implications for Research with Psychopathic Offenders. , 2006 .

[21]  M. L. Lambon Ralph,et al.  Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. , 2006, Brain : a journal of neurology.

[22]  A R Damasio,et al.  Developmental consequences of childhood frontal lobe damage. , 1992, Archives of neurology.

[23]  Christopher J. Patrick,et al.  Handbook of Psychopathy , 2007 .

[24]  Todd Lencz,et al.  Volume Reduction in Prefrontal Gray Matter in Unsuccessful Criminal Psychopaths , 2005, Biological Psychiatry.

[25]  Sasha Bozeat,et al.  Which neuropsychiatric and behavioural features distinguish frontal and temporal variants of frontotemporal dementia from Alzheimer's disease? , 2000, Journal of neurology, neurosurgery, and psychiatry.

[26]  Manuel F. Casanova,et al.  Reduced temporal lobe volume in early onset conduct disorder , 2004, Psychiatry Research: Neuroimaging.

[27]  Peter F. Liddle,et al.  Temporal lobe abnormalities in semantic processing by criminal psychopaths as revealed by functional magnetic resonance imaging , 2004, Psychiatry Research: Neuroimaging.

[28]  D. Kosson,et al.  Response perseveration in psychopaths. , 1987, Journal of abnormal psychology.

[29]  H. Damasio,et al.  Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. , 2000, Brain : a journal of neurology.

[30]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

[31]  David S Kosson,et al.  Factor structure of the Hare Psychopathy Checklist: Youth Version (PCL: YV) in incarcerated adolescents. , 2006, Psychological assessment.

[32]  A. Damasio,et al.  Preserved access and processing of social knowledge in a patient with acquired sociopathy due to ventromedial frontal damage , 1991, Neuropsychologia.

[33]  T. Insel,et al.  Subcortical projections of area 25 (subgenual cortex) of the macaque monkey , 2000, The Journal of comparative neurology.

[34]  R. Evans.  An Odd Kind of Fame: Stories of Phineas Gage , 2001 .

[35]  Friedrich Lösel,et al.  Psychopathy, risk taking, and attention: a differentiated test of the somatic marker hypothesis. , 2004, Journal of abnormal psychology.

[36]  Robert Kurzban,et al.  The neurobiology of trust. , 2008, Annals of the New York Academy of Sciences.

[37]  J. Ogloff,et al.  Psychopathy/antisocial personality disorder conundrum. , 2006, The Australian and New Zealand journal of psychiatry.

[38]  J. Monahan,et al.  Rethinking Risk Assessment: The MacArthur Study of Mental Disorder and Violence , 2001 .

[39]  Rex E. Jung,et al.  Structural brain variation and general intelligence , 2004, NeuroImage.

[40]  Michael Erb,et al.  Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study. , 2005, Archives of general psychiatry.

[41]  T. Noll,et al.  Violent and sexual offences: a validation of the predictive quality of the PCL:SV in Switzerland. , 2007, International journal of law and psychiatry.

[42]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[43]  J. Newman,et al.  Testing Damasio's somatic marker hypothesis with psychopathic individuals: risk takers or risk averse? , 1999, Journal of abnormal psychology.

[44]  A. Raine,et al.  Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. , 2000, Archives of general psychiatry.

[45]  Robert L. Spitzer,et al.  Global Assessment of Functioning (GAF) Scale , 1996 .

[46]  D. N. Pandya,et al.  Insular interconnections with the amygdala in the rhesus monkey , 1981, Neuroscience.

[47]  Sheilagh Hodgins,et al.  Ventral frontal deficits in psychopathy: Neuropsychological test findings , 1995, Neuropsychologia.

[48]  R. Hare,et al.  Structural models of psychopathy , 2005, Current psychiatry reports.

[49]  John Ashburner,et al.  Changes in cerebral morphology consequent to peripheral autonomic denervation , 2001, NeuroImage.

[50]  Jorge Moll,et al.  PSYCHOPATHY IN COMMUNITY PSYCHIATRIC PATIENTS IN BRAZIL , 2008 .

[51]  J. Grafman,et al.  The neural basis of human moral cognition , 2005, Nature Reviews Neuroscience.

[52]  P. Eslinger,et al.  Frontopolar and anterior temporal cortex activation in a moral judgment task: preliminary functional MRI results in normal subjects. , 2001, Arquivos de neuro-psiquiatria.

[53]  R. Nitrini,et al.  Incidence of Dementia in a Community-Dwelling Brazilian Population , 2004, Alzheimer disease and associated disorders.

[54]  M S Mega,et al.  The limbic system: an anatomic, phylogenetic, and clinical perspective. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[55]  Hannu J. Aronen,et al.  Psychopathy and the posterior hippocampus , 2001, Behavioural Brain Research.

[56]  Daniel Tranel,et al.  Asymmetric Functional Roles of Right and Left Ventromedial Prefrontal Cortices in Social Conduct, Decision-Making, and Emotional Processing , 2002, Cortex.

[57]  L Cipolotti,et al.  Impaired social response reversal. A case of 'acquired sociopathy'. , 2000, Brain : a journal of neurology.

[58]  Robert Plomin,et al.  Evidence for substantial genetic risk for psychopathy in 7-year-olds. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[59]  J. Decety,et al.  The Role of the Right Temporoparietal Junction in Social Interaction: How Low-Level Computational Processes Contribute to Meta-Cognition , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[60]  Laura S. Guy,et al.  Examining the utility of the PCL:SV as a screening measure using competing factor models of psychopathy. , 2006, Psychological assessment.

[61]  M. Dolan,et al.  Theory of mind and mentalizing ability in antisocial personality disorders with and without psychopathy , 2004, Psychological Medicine.

[62]  Masatoshi Itoh,et al.  Thinking of the future and past: the roles of the frontal pole and the medial temporal lobes , 2003, NeuroImage.

[63]  Jean-Pierre Guay,et al.  A taxometric analysis of the latent structure of psychopathy: evidence for dimensionality. , 2007, Journal of abnormal psychology.

[64]  Kent A. Kiehl,et al.  A cognitive neuroscience perspective on psychopathy: Evidence for paralimbic system dysfunction , 2006, Psychiatry Research.

[65]  Vanessa Sluming,et al.  Voxel-based morphometry and stereology provide convergent evidence of the importance of medial prefrontal cortex for fluid intelligence in healthy adults , 2005, NeuroImage.

[66]  A. Damasio,et al.  Severe disturbance of higher cognition after bilateral frontal lobe ablation , 1985, Neurology.

[67]  R. Hare,et al.  Psychopathy in a Civil Psychiatric Outpatient Sample , 2008 .

[68]  F Fazio,et al.  Brain abnormalities underlying altered activation in dyslexia: a voxel based morphometry study. , 2005, Brain : a journal of neurology.

[69]  H. Cleckley,et al.  The mask of sanity. , 1942, Postgraduate medicine.

[70]  Jordan Grafman,et al.  Social concepts are represented in the superior anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

[71]  Shelley L. Brown,et al.  The assessment of psychopathy in male and female noncriminals: Reliability and validity , 1996 .

[72]  L. Young,et al.  The neurobiology of pair bonding , 2004, Nature Neuroscience.

[73]  Jorge Moll,et al.  Morals and the human brain: a working model. , 2003, Neuroreport.

[74]  Robert D. Hare,et al.  The Hare Psychopathy Checklist-Revised , 1996 .

[75]  M. Dolan,et al.  Serotonergic and cognitive impairment in impulsive aggressive personality disordered offenders: are there implications for treatment? , 2002, Psychological Medicine.

[76]  J. Grafman,et al.  Human fronto–mesolimbic networks guide decisions about charitable donation , 2006, Proceedings of the National Academy of Sciences.

[77]  Glenn D. Walters,et al.  The Latent Structure of Psychopathy , 2007, Assessment.

[78]  J. Ringman,et al.  Pedophilia and temporal lobe disturbances. , 2000, The Journal of neuropsychiatry and clinical neurosciences.