Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: A meta-analysis

Brain-imaging studies suggest that antisocial and violent behavior is associated with structural and functional deficits in the prefrontal cortex, but there is heterogeneity in findings and it is unclear whether findings apply to psychopaths, non-violent offenders, community-based samples, and studies employing psychiatric controls. A meta-analysis was conducted on 43 structural and functional imaging studies, and the results show significantly reduced prefrontal structure and function in antisocial individuals. Effect sizes were significant for both structural and functional studies. With minor exceptions, no statistically significant moderating effects of sample characteristics and methodological variables were observed. Findings were localized to the right orbitofrontal cortex, right anterior cingulate cortex, and left dorsolateral prefrontal cortex. Findings confirm the replicability of prefrontal structural and functional impairments in antisocial populations and highlight the involvement of orbitofrontal, dorsolateral frontal, and anterior cingulate cortex in antisocial behavior.

[1]  J. Lieberman,et al.  Quantitative MRI measures of orbitofrontal cortex in patients with chronic schizophrenia or schizoaffective disorder , 2005, Psychiatry Research: Neuroimaging.

[2]  Michael Erb,et al.  Brain circuits involved in emotional learning in antisocial behavior and social phobia in humans , 2002, Neuroscience Letters.

[3]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Nora D. Volkow,et al.  Brain glucose metabolism in violent psychiatric patients: a preliminary study , 1995, Psychiatry Research: Neuroimaging.

[5]  R. McCarley,et al.  MRI anatomy of schizophrenia , 1999, Biological Psychiatry.

[6]  S. Lilienfeld,et al.  Development and preliminary validation of a self-report measure of psychopathic personality traits in noncriminal populations. , 1996, Journal of personality assessment.

[7]  J. Kashani,et al.  Risk Factors in Childhood That Lead to the Development of Conduct Disorder and Antisocial Personality Disorder , 2001, Child psychiatry and human development.

[8]  Kevin Dunbar,et al.  The Effects of Frontal Lobe Lesions on Goal Achievement in the Water Jug Task , 2001, Journal of Cognitive Neuroscience.

[9]  Jay Brand,et al.  File Drawer Problem , 2022, The SAGE Encyclopedia of Research Design.

[10]  A. Raine Biosocial Studies of Antisocial and Violent Behavior in Children and Adults: A Review , 2002, Journal of abnormal child psychology.

[11]  R. Orwin A fail-safe N for effect size in meta-analysis. , 1983 .

[12]  T. Sharma,et al.  Volumetric structural brain abnormalities in men with schizophrenia or antisocial personality disorder , 2006, Behavioural Brain Research.

[13]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[14]  Adrianna Mendrek,et al.  Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging , 2001, Biological Psychiatry.

[15]  G. Schellenberg,et al.  Developmental and vascular risk factors for Alzheimer's disease , 2005, Neurobiology of Aging.

[16]  R. Riascos,et al.  PET and SPECT in Drug and Substance Abuse , 2005, Topics in magnetic resonance imaging : TMRI.

[17]  E. Gorenstein,et al.  Disinhibitory psychopathology: a new perspective and a model for research. , 1980, Psychological review.

[18]  M. Karataş,et al.  Single Photon Emission Computerised Tomography in Chronic Alcoholism , 1996, British Journal of Psychiatry.

[19]  D. Stoff,et al.  Aggression and Violence: Genetic, Neurobiological, and Biosocial Perspectives , 1996 .

[20]  F. Mishkin,et al.  Left frontotemporal hypoperfusion is associated with aggression in patients with dementia. , 2000, Archives of neurology.

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

[22]  Karsten Specht,et al.  Brain localization of attentional control in different age groups by combining functional and structural MRI , 2004, NeuroImage.

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

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

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

[26]  Abigail A. Baird,et al.  Functional differences among those high and low on a trait measure of psychopathy , 2004, Biological Psychiatry.

[27]  Hiroshi Matsuda,et al.  Relationship between antisocial behavior and regional cerebral blood flow in frontotemporal dementia , 2006, NeuroImage.

[28]  L. Hedges,et al.  Statistical Methods for Meta-Analysis , 1987 .

[29]  R. Rosenthal The file drawer problem and tolerance for null results , 1979 .

[30]  Adrian Raine,et al.  Neural foundations to moral reasoning and antisocial behavior. , 2006, Social cognitive and affective neuroscience.

[31]  H. Anckarsäter Central nervous changes in social dysfunction: Autism, aggression, and psychopathy , 2006, Brain Research Bulletin.

[32]  M. Schwab-Stone,et al.  Antisocial behaviour and mental health , 2002, European Child & Adolescent Psychiatry.

[33]  S. Charles Schulz,et al.  Positron-Emission Tomography and Personality Disorders , 1994, Neuropsychopharmacology.

[34]  R. Davidson,et al.  Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence. , 2000, Science.

[35]  D Yves von Cramon,et al.  Decision-making and the frontal lobes , 2006, Current opinion in neurology.

[36]  Monika Sommer,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 , 2003, Biological Psychiatry.

[37]  Faith M. Gunning-Dixon,et al.  Prefrontal volumes in habitually violent subjects with antisocial personality disorder and type 2 alcoholism , 2002, Psychiatry Research: Neuroimaging.

[38]  Mark Slifstein,et al.  Brain serotonin transporter distribution in subjects with impulsive aggressivity: a positron emission study with [11C]McN 5652. , 2005, The American journal of psychiatry.

[39]  E. Rolls,et al.  Reward-related Reversal Learning after Surgical Excisions in Orbito-frontal or Dorsolateral Prefrontal Cortex in Humans , 2004, Journal of Cognitive Neuroscience.

[40]  A. Bechara The role of emotion in decision-making: Evidence from neurological patients with orbitofrontal damage , 2004, Brain and Cognition.

[41]  R S Menon,et al.  Investigation of BOLD contrast in fMRI using multi‐shot EPI , 1997, NMR in biomedicine.

[42]  J Currie,et al.  Goal-directed selective attention and response competition monitoring: evidence from unilateral parietal and anterior cingulate lesions. , 2000, Neuropsychology.

[43]  Leif Hultin,et al.  Reduced frontotemporal perfusion in psychopathic personality , 2002, Psychiatry Research: Neuroimaging.

[44]  D. Stuss,et al.  Stroop performance in focal lesion patients: dissociation of processes and frontal lobe lesion location , 2001, Neuropsychologia.

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

[46]  R. Blair,et al.  Neurocognitive models of aggression, the antisocial personality disorders, and psychopathy , 2001, Journal of neurology, neurosurgery, and psychiatry.

[47]  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.

[48]  M. Castillo,et al.  Magnetic Resonance Imaging Findings in Substance Abuse: Alcohol and Alcoholism and Syndromes Associated With Alcohol Abuse , 2005, Topics in magnetic resonance imaging : TMRI.

[49]  R. Hare,et al.  A brain imaging (single photon emission computerized tomography) study of semantic and affective processing in psychopaths , 1997, Biological Psychiatry.

[50]  F. Poustka,et al.  Reduced anterior cingulate activation in aggressive children and adolescents during affective stimulation: association with temperament traits. , 2007, Journal of psychiatric research.

[51]  Chris A. Johnson,et al.  The Relationship Between Structural and Functional Alterations in Glaucoma: A Review , 2000, Seminars in ophthalmology.

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

[53]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[54]  T. Sharma,et al.  Association between violent behaviour and impaired prepulse inhibition of the startle response in antisocial personality disorder and schizophrenia , 2005, Behavioural Brain Research.

[55]  A. Raine,et al.  Functional neuroanatomy of psychopathy , 2008 .

[56]  A. Damasio Descartes' error: emotion, reason, and the human brain. avon books , 1994 .

[57]  R. Thisted,et al.  Brain SPECT findings and aggressiveness. , 1996, Annals of clinical psychiatry : official journal of the American Academy of Clinical Psychiatrists.

[58]  Victoria Arango,et al.  Effects of sex, age, and aggressive traits in man on brain serotonin 5-HT1A receptor binding potential measured by PET using [C-11]WAY-100635 , 2002, Brain Research.

[59]  John S Duncan,et al.  Reduction of frontal neocortical grey matter associated with affective aggression in patients with temporal lobe epilepsy: an objective voxel by voxel analysis of automatically segmented MRI , 2000, Journal of neurology, neurosurgery, and psychiatry.

[60]  S. Ekholm,et al.  Reduced regional cerebral blood flow in non-psychotic violent offenders , 2000, Psychiatry Research: Neuroimaging.

[61]  E. Hoffman,et al.  Calculation of positron range and its effect on the fundamental limit of positron emission tomography system spatial resolution. , 1999, Physics in medicine and biology.

[62]  S. Patz,et al.  Orbitofrontal correlates of aggression and impulsivity in psychiatric patients , 2006, Psychiatry Research: Neuroimaging.

[63]  K. Phan,et al.  Amygdala and Orbitofrontal Reactivity to Social Threat in Individuals with Impulsive Aggression , 2007, Biological Psychiatry.

[64]  T. Moffitt,et al.  Neuropsychological and neuroimaging studies of juvenile delinquency and adult criminal behavior. , 1997 .

[65]  T. G. Campbell The Best of a Bad Bunch: The Ventromedial Prefrontal Cortex and Dorsal Anterior Cingulate Cortex in Decision-Making , 2007, The Journal of Neuroscience.

[66]  Mark J Lowe,et al.  Media Violence Exposure and Frontal Lobe Activation Measured by Functional Magnetic Resonance Imaging in Aggressive and Nonaggressive Adolescents , 2005, Journal of computer assisted tomography.

[67]  Adrian Raine,et al.  The Psychopathology of Crime: Criminal Behavior as a Clinical Disorder , 1993 .

[68]  M. Hoptman,et al.  Frontal white matter microstructure, aggression, and impulsivity in men with schizophrenia: a preliminary study , 2002, Biological Psychiatry.

[69]  Adrian Raine,et al.  Brain abnormalities in murderers indicated by positron emission tomography , 1997, Biological Psychiatry.

[70]  A. Damasio Descartes’ Error. Emotion, Reason and the Human Brain. New York (Grosset/Putnam) 1994. , 1994 .

[71]  L. Deecke,et al.  Behavioural and psychosocial sequelae of severe closed head injury and regional cerebral blood flow: a SPECT study. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[72]  Philipp Sterzer,et al.  Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder , 2005, Biological Psychiatry.

[73]  V. Mathews,et al.  Adolescents with Disruptive Behavior Disorder Investigated Using an Optimized MR Diffusion Tensor Imaging Protocol , 2005, Annals of the New York Academy of Sciences.

[74]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[75]  H. Critchley,et al.  Prefrontal and medial temporal correlates of repetitive violence to self and others , 2000, Biological Psychiatry.

[76]  R. Rosenthal Combining results of independent studies. , 1978 .

[77]  R Rosenthal,et al.  Meta‐analysis: a review. , 1991, Psychosomatic medicine.

[78]  Adham Mancini-Marı̈e,et al.  Violent persons with schizophrenia and comorbid disorders: A functional magnetic resonance imaging study , 2007, Schizophrenia Research.

[79]  G. Pagnoni,et al.  Neural Correlates of Social Cooperation and Non-Cooperation as a Function of Psychopathy , 2007, Biological Psychiatry.

[80]  D. Kosson Psychopathy and dual-task performance under focusing conditions. , 1996, Journal of abnormal psychology.

[81]  M. Behen,et al.  Bilateral Medial Prefrontal and Temporal Neocortical Hypometabolism in Children with Epilepsy and Aggression , 2001, Epilepsia.

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

[83]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[84]  C. Li,et al.  Antisocial personality and stress-induced brain activation in cocaine-dependent patients , 2006, Neuroreport.

[85]  A. Cantagallo,et al.  Emotional impairment after right orbitofrontal lesion in a patient without cognitive deficits. , 1999, Neuroreport.

[86]  Wolfgang Grodd,et al.  Functional Imaging of Conditioned Aversive Emotional Responses in Antisocial Personality Disorder , 2000, Neuropsychobiology.

[87]  Paul J. Eslinger,et al.  Long-term psychological consequences of childhood frontal lobe lesion in patient DT , 1992, Brain and Cognition.

[88]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

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

[90]  D. Stoff,et al.  Handbook of antisocial behavior , 1997 .

[91]  B. Price,et al.  Neuropsychiatry of frontal lobe dysfunction in violent and criminal behaviour: a critical review , 2001, Journal of neurology, neurosurgery, and psychiatry.

[92]  Andrea L Glenn,et al.  Brain abnormalities in antisocial individuals: implications for the law. , 2008, Behavioral sciences & the law.

[93]  G. Fong,et al.  A select group of perpetrators of domestic violence: evidence of decreased metabolism in the right hypothalamus and reduced relationships between cortical/subcortical brain structures in position emission tomography , 2004, Psychiatry Research: Neuroimaging.