[Skip to Content]
Access to paid content on this site is currently suspended due to excessive activity being detected from your IP address 23.23.54.109. Please contact the publisher to request reinstatement.
Sign In
Individual Sign In
Create an Account
Institutional Sign In
OpenAthens Shibboleth
[Skip to Content Landing]
Download PDF
Figure 1.
The amygdala was traced in high-resolution T1-weighted images using the software MultiTracer (http://air.bmap.ucla.edu/MultiTracer). Tracing was performed in contiguous coronal slices (A-C showing posterior to anterior) while referencing orthogonal sagittal (D) and transverse (E) planes to confirm the correct identification of anatomical boundaries. Even though only the tracings of the right amygdala are illustrated, the left amygdala was traced following the same protocol.

The amygdala was traced in high-resolution T1-weighted images using the software MultiTracer (http://air.bmap.ucla.edu/MultiTracer). Tracing was performed in contiguous coronal slices (A-C showing posterior to anterior) while referencing orthogonal sagittal (D) and transverse (E) planes to confirm the correct identification of anatomical boundaries. Even though only the tracings of the right amygdala are illustrated, the left amygdala was traced following the same protocol.

Figure 2.
The amygdala nuclei and significant regional amygdala surface deformations. A, Schematic representation of the amygdala nuclei is mapped onto the 3-dimensional left and right amygdala surfaces. Structural variation of the human amygdala and individual differences in the relative position of the amygdala nuclei across the surface do not allow the locations of the amygdala nuclei to be determined with a high degree of accuracy in imaging data. Thus, the boundaries of the different subnuclei are approximations based on an extrapolation of the relative nuclei positions derived from the atlas of Mai et al. AAA indicates anterior amygdaloid area; AB, accessory basal nucleus; ACo, anterior cortical nucleus; AI, amygdaloid island; BL, basolateral nucleus; BM, basomedial nucleus; Ce, central nucleus; La, lateral nucleus; MeA, medial amygdaloid nucleus; PACl, preamygdalar claustrum; PCo, posterior cortical nucleus; PHA, parahippocampal-amygdaloid transition area; PirT, piriform cortex. B, Statistical maps showing significant regional amygdala surface deformations in individuals with psychopathy (n = 27) compared with healthy controls (n = 32) as encoded by the color bar (uncorrected P value). No surface expansion in the amygdala in individuals with psychopathy was observed.

The amygdala nuclei and significant regional amygdala surface deformations. A, Schematic representation of the amygdala nuclei is mapped onto the 3-dimensional left and right amygdala surfaces. Structural variation of the human amygdala and individual differences in the relative position of the amygdala nuclei across the surface do not allow the locations of the amygdala nuclei to be determined with a high degree of accuracy in imaging data. Thus, the boundaries of the different subnuclei are approximations based on an extrapolation of the relative nuclei positions derived from the atlas of Mai et al.53 AAA indicates anterior amygdaloid area; AB, accessory basal nucleus; ACo, anterior cortical nucleus; AI, amygdaloid island; BL, basolateral nucleus; BM, basomedial nucleus; Ce, central nucleus; La, lateral nucleus; MeA, medial amygdaloid nucleus; PACl, preamygdalar claustrum; PCo, posterior cortical nucleus; PHA, parahippocampal-amygdaloid transition area; PirT, piriform cortex. B, Statistical maps showing significant regional amygdala surface deformations in individuals with psychopathy (n = 27) compared with healthy controls (n = 32) as encoded by the color bar (uncorrected P value). No surface expansion in the amygdala in individuals with psychopathy was observed.

Figure 3.
Amygdala volumes in psychopathic individuals and normal controls, with total brain volume as a covariate. The vertical lines represent the standard error. The group mean (SD) volume is indicated.

Amygdala volumes in psychopathic individuals and normal controls, with total brain volume as a covariate. The vertical lines represent the standard error. The group mean (SD) volume is indicated.

Figure 4.
Statistical maps showing significant negative correlations between the amygdala surface structure and total psychopathy (A) and interpersonal (B), affective (C), lifestyle (D), and antisocial (E) facet scores across the entire sample of 59 subjects. The uncorrected P values corresponding to significant r values are encoded by the color bar. The regional deformations were confirmed by permutations indicating an overall pattern of significant correlations between deformations in the amygdala and the increase in the total and facet scores.

Statistical maps showing significant negative correlations between the amygdala surface structure and total psychopathy (A) and interpersonal (B), affective (C), lifestyle (D), and antisocial (E) facet scores across the entire sample of 59 subjects. The uncorrected P values corresponding to significant r values are encoded by the color bar. The regional deformations were confirmed by permutations indicating an overall pattern of significant correlations between deformations in the amygdala and the increase in the total and facet scores.

Table 1. 
Demographic, Cognitive, and Diagnostic Measures for Psychopathy and Control Groups
Demographic, Cognitive, and Diagnostic Measures for Psychopathy and Control Groups
Table 2. 
Correlations Between Amygdala Volumes and the Total and 4 Facet Scores of Psychopathy in the Entire Sample of 59, Controlling for Whole-Brain Volume
Correlations Between Amygdala Volumes and the Total and 4 Facet Scores of Psychopathy in the Entire Sample of 59, Controlling for Whole-Brain Volume
1.
Cleckley  H The Mask of Sanity.  St Louis, MO Mosby1941;
2.
Cooke  DJMichie  CHart  SD Facets of clinical psychopathy: toward clearer measurement. Patrick  CJHandbook of Psychopathy. New York, NY The Guilford Press2005;
3.
Hare  RD Manual for the Hare Psychopathy Checklist–Revised.  Toronto, ON, Canada Multi-Health Systems1991;
4.
Patrick  CJ Emotional processes in psychopathy. Raine  ASanmartín  JViolence and Psychopathy. New York, NY Kluwer Academic/Plenum Publishers2001;
5.
Arnett  PA Autonomic responsivity in psychopaths: a critical review and theoretical proposal. Clin Psychol Rev 1997;17 (8) 903- 936
PubMedArticle
6.
Kiehl  KAHare  RD McDonald  JJBrink  J Semantic and affective processing in psychopaths: an event-related potential (ERP) study. Psychophysiology 1999;36 (6) 765- 774
PubMedArticle
7.
Patrick  CJBradley  MMLang  PJ Emotion in the criminal psychopath: startle reflex modulation. J Abnorm Psychol 1993;102 (1) 82- 92
PubMedArticle
8.
Raine  A Evoked potentials and psychopathy. Int J Psychophysiol 1989;8 (1) 1- 16
PubMedArticle
9.
Raine  A Crime, conditioning, and arousal. Nyborg  HThe Scientific Study of Human Nature Tribute to Hanes J. Eysenck. Oxford, England: Elsevier1997;
10.
Stanford  MSHouston  RJBarratt  ES Psychophysiological correlates of psychopathic disorders. Felthous  ARSaß  HInternational Handbook on Psychopathic Disorders and the Law. Hoboken, NJ John Wiley & Sons Inc2007;
11.
Patrick  CJ Emotion and psychopathy: startling new insights. Psychophysiology 1994;31 (4) 319- 330
PubMedArticle
12.
Patrick  CJCuthbert  BNLang  PJ Emotion in the criminal psychopath: fear image processing. J Abnorm Psychol 1994;103 (3) 523- 534
PubMedArticle
13.
Williamson  SHarpur  TJHare  RD Abnormal processing of affective words by psychopaths. Psychophysiology 1991;28 (3) 260- 273
PubMedArticle
14.
Adolphs  RTranel  DDamasio  HDamasio  AR Fear and the human amygdala. J Neurosci 1995;15 (9) 5879- 5891
PubMed
15.
Adolphs  RTranel  DHamann  SYoung  AWCalder  AJPhelps  EAAnderson  ALee  GPDamasio  AR Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 1999;37 (10) 1111- 1117
PubMedArticle
16.
Brothers  LRing  BKling  A Response of neurons in the macaque amygdala to complex social stimuli. Behav Brain Res 1990;41 (3) 199- 213
PubMedArticle
17.
Kling  AGreen  PC Effects of neonatal amygdalectomy in the maternally reared and maternally deprived monkey. Nature 1967;213 (5077) 742- 743
PubMedArticle
18.
Phelps  EA Emotion and cognition: insights from studies of the human amygdala. Annu Rev Psychol 2006;5727- 53
PubMedArticle
19.
Adolphs  RTranel  DDamasio  HDamasio  A Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 1994;372 (6507) 669- 672
PubMedArticle
20.
Blair  RJ The roles of orbitofrontal cortex in the modulation of antisocial behavior. Brain Cogn 2004;55 (1) 198- 208
PubMedArticle
21.
Baxter  MGMurray  EA The amygdala and reward. Nat Rev Neurosci 2002;3 (7) 563- 573
PubMedArticle
22.
Blair  RJR The amygdala and ventromedial prefrontal cortex in morality and psychopathy. Trends Cogn Sci 2007;11 (9) 387- 392
PubMedArticle
23.
Davis  M The role of the amygdala in conditioned fear. Aggleton  JPThe Amygdala Neurobiological Aspects of Emotion, Memory and Mental Dysfunction. New York, NY: Wiley-Liss1992;
24.
Everitt  BJCardinal  RNParkinson  JARobbins  TW Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning. Ann N Y Acad Sci 2003;985233- 250
PubMedArticle
25.
Holland  PCGallagher  M Amygdala-frontal interactions and reward expectancy. Curr Opin Neurobiol 2004;14 (2) 148- 155
PubMedArticle
26.
LeDoux  JE The Emotional Brain.  New York, NY Simon & Schuster1996;
27.
Raine  AYang  Y Neural foundations to moral reasoning and antisocial behavior. Soc Cogn Affect Neurosci 2006;1 (3) 203- 213
PubMedArticle
28.
Knapska  ERadwanska  KWerka  TKaczmarek  L Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. Physiol Rev 2007;87 (4) 1113- 1173
PubMedArticle
29.
Sah  PFaber  ESLopez De Armentia  MPower  J The amygdaloid complex: anatomy and physiology. Physiol Rev 2003;83 (3) 803- 834
PubMed
30.
Balleine  BWKillcross  S Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci 2006;29 (5) 272- 279
PubMedArticle
31.
Blair  RJJones  LClark  FSmith  M The psychopathic individual: a lack of responsiveness to distress cues? Psychophysiology 1997;34 (2) 192- 198
PubMedArticle
32.
Damasio  A Descartes' Error: Emotion, Reason, and the Human Brain.  New York, NY GP Putnam's Sons1994;
33.
Kiehl  KA A cognitive neuroscience perspective on psychopathy: evidence for paralimbic system dysfunction. Psychiatry Res 2006;142 (2-3) 107- 128
PubMedArticle
34.
Yang  YRaine  A Functional and structural brain imaging research on psychopathy. Felthous  AHSass  HInternational Handbook on Psychopathic Disorders and the Law. Hoboken, NJ Wiley2006;
35.
Hare  RD Manual for the Revised Psychopathy Checklist. 2nd ed. Toronto, ON, Canada Multi-Health Systems2003;
36.
Raine  ALencz  TBihrle  SLaCasse  LColletti  P Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. Arch Gen Psychiatry 2000;57 (2) 119- 127, discussion 128-129
PubMedArticle
37.
Kosson  DSSteuerwald  BLForth  AEKirkhart  KJ A new method for assessing the interpersonal behavior of psychopathic individuals: preliminary validation studies. Psychol Assess 1997;9 (2) 89- 101Article
38.
Elliott  DSAgeton  SSHuizinga  DKnowles  BACanter  RJ The Prevalence and Incidence of Delinquent Behavior: 1976-1980—National Estimates of Delinquent Behavior by Sex, Race, Social Class and Other Selected Variables.  Boulder, CO Behavior Research Institute1983;National Youth Survey Report No. 26
39.
First  MBSpitzer  RLGibbon  MWilliams  JBW Structured Clinical Interview for Axis I DSM-IV Disorders (SCID, Version 2.0).  New York New York State Psychiatric Institute1994;
40.
First  MBSpitzer  RLGibbon  MWilliams  JBWBenjamin  L Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II, Version 2.0).  New York New York State Psychiatric Institute1994;
41.
Yang  YRaine  ALencz  TBihrle  SLaCasse  LColletti  P Volume reduction in prefrontal gray matter in unsuccessful criminal psychopaths. Biol Psychiatry 2005;57 (10) 1103- 1108
PubMedArticle
42.
Raine  AIshikawa  SSArce  ELencz  TKnuth  KHBihrle  SLaCasse  LColletti  P Hippocampal structural asymmetry in unsuccessful psychopaths. Biol Psychiatry 2004;55 (2) 185- 191
PubMedArticle
43.
Raine  ALencz  TTaylor  KHellige  JBBihrle  SLacasse  LLee  MIshikawa  SColletti  P Corpus callosum abnormalities in psychopathic antisocial individuals. Arch Gen Psychiatry 2003;60 (11) 1134- 1142
PubMedArticle
44.
Harris  GTRice  MEQuinsey  VL Psychopathy as a taxon: evidence that psychopaths are a discrete class. J Consult Clin Psychol 1994;62 (2) 387- 397
PubMedArticle
45.
Hollingshead  AB Four Factor Index of Social Status.  New Haven, CT Department of Sociology, Yale University1975;
46.
Wechsler  D Wechsler Adult Intelligence Scale–Revised.  San Antonio, TX Psychological Corp1981;
47.
Bryden  MP Measuring handedness with questionnaires. Neuropsychologia 1977;15 (4-5) 617- 624
PubMedArticle
48.
Sled  JGPike  GB Standing-wave and RF penetration artifacts caused by elliptic geometry: an electrodynamic analysis of MRI. IEEE Trans Med Imaging 1998;17 (4) 653- 662
PubMedArticle
49.
Mazziotta  JCToga  AWEvans  AFox  PLancaster  JThe International Consortium for Brain Mapping (ICBM), A probabilistic atlas of the human brain: theory and rationale for its development. Neuroimage 1995;2 (2) 89- 101
PubMedArticle
50.
Narr  KLThompson  PMSharma  TMoussai  JBlanton  RAnvar  BEdris  AKrupp  RRayman  JKhaledy  MToga  AW Three-dimensional mapping of temporo-limbic regions and the lateral ventricles in schizophrenia: gender effects. Biol Psychiatry 2001;50 (2) 84- 97
PubMedArticle
51.
Bartzokis  GMintz  JMarx  POsborn  DGutkind  DChiang  FPhelan  CKMarder  SR Reliability of in vivo volume measures of hippocampus and other brain structures using MRI. Magn Reson Imaging 1993;11 (7) 993- 1006
PubMedArticle
52.
Levitt  JGBlanton  RECaplan  RAsarnow  RGuthrie  DToga  AWCapetillo-Cunliffe  L McCracken  JT Medial temporal lobe in childhood-onset schizophrenia. Psychiatry Res 2001;108 (1) 17- 27
PubMedArticle
53.
Mai  JKAssheuer  JPaxinos  G Atlas of the Human Brain.  San Diego, CA Academic Press1997;
54.
Yang  YRaine  ANarr  KLLencz  TLaCasse  LColletti  PToga  AW Localisation of increased prefrontal white matter in pathological liars. Br J Psychiatry 2007;190174- 175
PubMedArticle
55.
Ballmaier  MNarr  KLToga  AWElderkin-Thompson  VThompson  PMHamilton  LHaroon  EPham  DHeinz  AKumar  A Hippocampal morphology and distinguishing late-onset from early-onset elderly depression. Am J Psychiatry 2008;165 (2) 229- 237
PubMedArticle
56.
Narr  KLThompson  PMSzeszko  PRobinson  DJang  SWoods  RPKim  SHayashi  KMAsunction  DToga  AWBilder  RM Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage 2004;21 (4) 1563- 1575
PubMedArticle
57.
Thompson  PMHayashi  KMDe Zubicaray  GLJanke  ALRose  SESemple  JHong  MSHerman  DHGravano  DDoddrell  DMToga  AW Mapping hippocampal and ventricular change in Alzheimer's disease. Neuroimage 2004;22 (4) 1754- 1766
PubMedArticle
58.
Bullmore  ETSuckling  JOvermeyer  SRabe-Hesketh  STaylor  EBrammer  MJ Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 1999;18 (1) 32- 42
PubMedArticle
59.
Hitchcock  JDavis  M Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav Neurosci 1986;100 (1) 11- 22
PubMedArticle
60.
Machado  CJBachevalier  J The impact of selective amygdala, orbitofrontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behav Neurosci 2006;120 (4) 761- 786
PubMedArticle
61.
Kalin  NHShelton  SEDavidson  RJKelley  AE The primate amygdala mediates acute fear but not the behavioral physiological components of anxious temperament. J Neurosci 2001;21 (6) 2067- 2074
PubMed
62.
Izquierdo  ASuda  RKMurray  EA Comparison of the effects of bilateral orbital prefrontal cortex lesions and amygdala lesions on emotional responses in rhesus monkeys. J Neurosci 2005;25 (37) 8534- 8542
PubMedArticle
63.
Hare  HD Electrodermal and cardiovascular correlates of psychopathy. Hare  RDSchalling  DPsychopathic Behavioral Approaches to Research. New York, NY: Wiley1978;
64.
Marsh  AABlair  RJ Deficits in facial affect recognition among antisocial populations: a meta-analysis. Neurosci Biobehav Rev 2008;32 (3) 454- 465
PubMedArticle
65.
Adolphs  RBaron-Cohen  STranel  D Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci 2002;14 (8) 1264- 1274
PubMedArticle
66.
Anderson  AKSpencer  DDFulbright  RKPhelps  EA Contribution of the anteromedial temporal lobes to the evaluation of facial emotion. Neuropsychology 2000;14 (4) 526- 536
PubMedArticle
67.
Anderson  AKPhelps  EA Intact recognition of vocal expressions of fear following bilateral lesions of the human amygdala. Neuroreport 1998;9 (16) 3607- 3613
PubMedArticle
68.
Anderson  AKPhelps  EA Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 2001;411 (6835) 305- 309
PubMedArticle
69.
Broks  PYoung  AWMaratos  EJCoffey  PJCalder  AJIsaac  CLMayes  ARHodges  JRMontaldi  DCezayirli  ERoberts  NHadley  D Face processing impairments after encephalitis: amygdala damage and recognition of fear. Neuropsychologia 1998;36 (1) 59- 70
PubMedArticle
70.
Young  AWHellawell  DJVan De Wal  CJohnson  M Facial expression processing after amygdalotomy. Neuropsychologia 1996;34 (1) 31- 39
PubMedArticle
71.
Schmolck  HSquire  LR Impaired perception of facial emotions following bilateral damage to the anterior temporal lobe. Neuropsychology 2001;15 (1) 30- 38
PubMedArticle
72.
Hudson  LPMunoz  DGMiller  L McLachlan  RSGirvin  JPBlume  WT Amygdaloid sclerosis in temporal lobe epilepsy. Ann Neurol 1993;33 (6) 622- 631
PubMedArticle
73.
Miller  LA McLachlan  RSBouwer  MSHudson  LPMunoz  DG Amygdalar sclerosis: preoperative indicators and outcome after temporal lobectomy. J Neurol Neurosurg Psychiatry 1994;57 (9) 1099- 1105
PubMedArticle
74.
Guerreiro  CCendes  FLi  LMJones-Gotman  MAndermann  FDubeau  FPiazzini  AFeindel  W Clinical patterns of patients with temporal lobe epilepsy and pure amygdalar atrophy. Epilepsia 1999;40 (4) 453- 461
PubMedArticle
75.
Pitkänen  ATuunanen  JKälviäinen  RPartanen  KSalmenperä  T Amygdala damage in experimental and human temporal lobe epilepsy. Epilepsy Res 1998;32 (1-2) 233- 253
PubMedArticle
76.
Meyer  ABeck  EShepherd  M Unusually severe lesions in the brain following status epilepticus. J Neurol Neurosurg Psychiatry 1955;18 (1) 24- 33
PubMedArticle
77.
Margerison  JHCorsellis  JA Epilepsy and the temporal lobes: a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 1966;89 (3) 499- 530
PubMedArticle
78.
Houghton  JMBroks  PWing  AEldridge  PWalsh  RDavies  PJukes  RKuczynski  AReynders  H Does temporal lobe epilepsy impair the ability to recognize cues to the emotional state of others? Epilepsia 2000;41 ((suppl 7)) 249
79.
Adolphs  RTranel  DDamasio  AR The human amygdala in social judgment. Nature 1998;393 (6684) 470- 474
PubMedArticle
80.
Reynders  HJBroks  PDickson  JMLee  CETurpin  G Investigation of social and emotion information processing in temporal lobe epilepsy with ictal fear. Epilepsy Behav 2005;7 (3) 419- 429
PubMedArticle
81.
Plutchik  R Emotions and sociopathy. Behav Brain Sci 1995;18 (3) 570- 571Article
82.
Tiihonen  JHodgins  SVaurio  O Amygdaloid volume loss in psychopathy. Abstr Soc Neurosci 2000;2017
83.
Gordon  HLBaird  AAEnd  A Functional differences among those high and low on a trait measure of psychopathy. Biol Psychiatry 2004;56 (7) 516- 521
PubMedArticle
84.
Rilling  JKGlenn  ALJairam  MRPagnoni  GGoldsmith  DRElfenbein  HALilienfeld  SO Neural correlates of social cooperation and non-cooperation as a function of psychopathy. Biol Psychiatry 2007;61 (11) 1260- 1271
PubMedArticle
85.
Glenn  ALRaine  ASchug  RA The neural correlates of moral decision-making in psychopathy. Mol Psychiatry 2009;14 (1) 5- 6
PubMedArticle
86.
Anderson  AKPhelps  EA Expression without recognition: contributions of the human amygdala to emotional communication. Psychol Sci 2000;11 (2) 106- 111
PubMedArticle
87.
McGaugh  JL The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 2004;271- 28
PubMedArticle
88.
Sarter  MMarkowitsch  HJ Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations. Behav Neurosci 1985;99 (2) 342- 380
PubMedArticle
89.
Whalen  PJ The uncertainty of it all. Trends Cogn Sci 2007;11 (12) 499- 500
PubMedArticle
90.
Savander  VGo  CLedoux  JEPitkänen  A Intrinsic connections of the rat amygdaloid complex: projections originating in the basal nucleus. J Comp Neurol 1995;361 (2) 345- 368
PubMedArticle
Original Article
September 2009

Localization of Deformations Within the Amygdala in Individuals With Psychopathy

Author Affiliations

Author Affiliations: Laboratory of Neuro Imaging, Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles (Drs Yang, Narr, and Toga) and Department of Radiology, School of Medicine, University of Southern California (Dr Colletti), Los Angeles; and Department of Criminology, Psychiatry, and Psychology, University of Pennsylvania, Philadelphia (Dr Raine).

Arch Gen Psychiatry. 2009;66(9):986-994. doi:10.1001/archgenpsychiatry.2009.110
Abstract

Context  Despite the repeated findings of impaired fear conditioning and affective recognition in psychopathic individuals, there has been a paucity of brain imaging research on the amygdala and no evidence suggesting which regions within the amygdala may be structurally compromised in individuals with psychopathy.

Objective  To detect global and regional anatomical abnormalities in the amygdala in individuals with psychopathy.

Design  Cross-sectional design using structural magnetic resonance imaging.

Setting  Participants were recruited from high-risk communities (temporary employment agencies) in the Los Angeles, California, area and underwent imaging at a hospital research facility at the University of Southern California.

Participants  Twenty-seven psychopathic individuals as defined by the Hare Psychopathy Checklist–Revised and 32 normal controls matched on age, sex, and ethnicity.

Main Outcome Measures  Amygdala volumes were examined using traditional volumetric analyses and surface-based mesh modeling methods were used to localize regional surface deformations.

Results  Individuals with psychopathy showed significant bilateral volume reductions in the amygdala compared with controls (left, 17.1%; right, 18.9%). Surface deformations were localized in regions in the approximate vicinity of the basolateral, lateral, cortical, and central nuclei of the amygdala. Significant correlations were found between reduced amygdala volumes and increased total and facet psychopathy scores, with correlations strongest for the affective and interpersonal facets of psychopathy.

Conclusions  Results provide the first evidence, to our knowledge, of focal amygdala abnormalities in psychopathic individuals and corroborate findings from previous lesion studies. Findings support prior hypotheses of amygdala deficits in individuals with psychopathy and indicate that amygdala abnormalities contribute to emotional and behavioral symptoms of psychopathy.

Psychopathy is a clinical condition conceptualized by a combination of core psychopathic personalities (eg, shallow affect, conning and manipulative) and antisocial behavioral outcomes (eg, parasitic lifestyle, poor behavioral control).13 Psychopathic individuals are particularly viewed as having a specific emotional and interpersonal style that is characterized by the inability to recognize and experience the emotional significance of social events.4 It was suggested that as a result of their emotional impairments, individuals with psychopathy use a detached, predatory style of antisocial behavior as a strategy to meet their immediate needs without regard for the consequences.4 Consistent with the symptoms of psychopathy, one of the most robust findings in individuals with psychopathy is the abnormal psychophysiological responsivity during the viewing of emotional stimuli and aversive conditioning learning,510 suggesting possible deficits in the neurobiological system that governs emotional response, particularly negative emotions, such as fear and anger.1113

The amygdala has long been known as one of the most important components in the neural circuit underlying emotional processing.1418 An intact amygdala is found to be necessary for fear conditioning19; thus, impairments in this structure have been hypothesized to contribute to the well-replicated observations of poor fear conditioning in individuals with psychopathy.9,20 In addition, the amygdala is an important component of the neural systems subserving reward learning, social interaction, and moral emotion and reasoning,2126 where the ability to recognize the emotions signaled by facial expressions is crucial for making advantageous decisions in a complex social environment.19 Therefore, it has also been hypothesized that disturbances in amygdala structure or function may contribute to the social dysfunction and impaired moral decision making in individuals with psychopathy.27

Studies have revealed that the amygdala is not a homogeneous structure and can be differentiated into approximately 13 nuclei. Although the functional specificity of the nuclei in the human amygdala remains unclear, considerable evidence from animal studies suggests that several nuclei of the amygdala are involved in the processing of emotion.28,29 For example, the basolateral and lateral nuclei have been linked to the encoding of sensory-specific features, whereas the central nucleus has been associated with encoding the motivational or affective aspects.30 The importance of the amygdala and its subdivisions in emotional processing and social functioning has led to several predictions that global and regional deficits of the amygdala may contribute to features of psychopathy3134; however, to our knowledge, no study to date has examined the structural integrity of the amygdala in psychopathic individuals.

Using a community sample, we examined the structure of the amygdala in psychopathic and control groups. It was hypothesized that psychopathic individuals would show a global volume reduction in the amygdala and regional morphological alterations in the approximate locations of basolateral, lateral, and central nuclei. Furthermore, we examined correlations between the amygdala and degree of psychopathy using the 4-facet concept of psychopathy, which includes interpersonal (eg, superficial charm, manipulative), affective (eg, shallow affect, lack of remorse), lifestyle (eg, impulsivity, irresponsibility), and antisocial (eg, poor behavioral control, criminal versatility) facets.35 It was predicted that reduced amygdala volume would correlate more prominently with the core features of psychopathy (ie, interpersonal and affective facets) than the secondary features of antisocial behavior (ie, lifestyle and antisocial facets), which are more common in nonpsychopathic offenders and not as specific to the syndrome of psychopathy.

METHODS
PARTICIPANTS

Eighty-six subjects were recruited from 5 temporary employment agencies in Los Angeles, California.35 Samples from this community have been found to show relatively higher rates of psychopathy/antisocial personality.36 Psychopathy was assessed using the Hare Psychopathy Checklist–Revised (PCL-R)3,35 and supplemented by 5 sources of collateral data that included (1) the Interpersonal Measure of Psychopathy37 ratings; (2) self-reported crime and violence assessed using an adult extension36 of the National Youth Survey self-report delinquency measure38; (3) criminal history transcripts obtained from the Department of Justice; (4) data derived from, and behavioral observations made during, the Structured Clinical Interview for Axis I DSM-IV Disorders and Axis II Personality Disorders39,40; and (5) independent Interpersonal Measure of Psychopathy ratings made by 2 different laboratory assistants during separate phases of testing. A cutoff of 23 (high) and 15 (low) on the total PCL-R score was used to define psychopathy, resulting in a total of 27 individuals with psychopathy (PCL-R score range, 23-40) and 32 controls (PCL-R score range, 5-14). This cutoff was chosen to be consistent with our prior research on this sample36,4143 and is similar to the optimal cutoff suggested by taxometric analyses of the PCL-R.44 The general term of individuals with psychopathy is used in this article to refer to community individuals with a PCL-R score higher than 23. Demographic, cognitive, and diagnostic characteristic information were collected as follows: (1) age, sex, and ethnicity; (2) socioeconomic status45; (3) full-scale IQ as assessed by the Wechsler Adult Intelligence Scale–Revised46; (4) handedness as assessed by the abbreviated Oldfield Inventory47; (5) lifetime diagnosis of drug/alcohol dependence as assessed by the Structural Clinical Interview for Axis I DSM-IV Disorders39; and (6) the number of alcohol drinks used in the past month as assessed by the alcohol use questionnaire.36 Written informed consent was obtained from all subjects and the study was approved by the University of Southern California institutional review board.

MAGNETIC RESONANCE IMAGE ANALYSIS

Structural magnetic resonance images were collected on a 1.5-T Philips (Shelton, Connecticut) S15/ACS scanner (repetition time = 34 milliseconds, echo time = 12.4 milliseconds, voxel size = 0.9 × 0.9 × 1.7 mm).36 Before the delineation process, each image volume was first corrected for magnetic field inhomogeneities48 and head tilt and alignment by using 6-parameter rigid-body registrations.44 During the registration procedure, the image volumes were placed in a common coordinate space.49

The delineation of the amygdala was conducted by 2 independent technicians (premedical neuroscience trainees) who received extensive training on the delineation protocols under the supervision of one of us (Y.Y.). These 2 technicians, blind to group membership, traced the amygdala following a delineation protocol adopted from previously validated methods5052 and based on the atlas of the amygdala anatomy by Mai et al.53 The images were first resampled to 1-mm thickness to improve the visibility of anatomical details for identifying the structure. The amygdala was traced in coronal brain slices from posterior to anterior while using the digitized surface contours simultaneously displayed in both sagittal and transverse planes to facilitate a more accurate identification of the boundaries that separate the amygdala from surrounding structures (Figure 1). The amygdala was traced on magnified images (×4) to allow better precision in identifying the anatomical boundaries. Amygdala tracing in each hemisphere began when the structure appeared as a pebble of gray matter superior to the temporal horn of the lateral ventricle and inferior to the white matter of the parietal lobe. As the lateral ventricle moved to a more lateral position as the brain volumes moved anterior, the alveus appeared and was used as the inferior boundary that separates the amygdala from the hippocampus. The inferior boundary shifted to the temporal lobe white matter when the alveus was no longer visible. The tracing of the amygdala was continued anteriorly until the lateral ventricle completely separated the temporal lobe from the rest of the cerebrum. For each subject, right and left amygdala volumes were extracted using these tracings. To assess interrater reliability, 10 different randomly selected cases were traced and the interrater intraclass correlation coefficients for amygdala volumes ranged between 0.91 and 0.95. Whole-brain volumes, obtained as previously described,54 were retained for use as covariates to control for individual differences in brain size in analyses of amygdala morphology.

SURFACE-BASED MESH AVERAGING

Surface meshes were constructed for the amygdala using surface-based anatomical modeling, and skeletonizing methods were used to identify regional morphological changes of the amygdala.55 The surface contours representing each individual's left or right amygdala were made spatially uniform within and across subjects, where each surface was made to represent 15 000 surface points or nodes. Radial distances from the central core (medial axis) of each amygdala to the spatially normalized surface points were then computed within subjects. These distances obtained at each spatially equivalent amygdala surface point were then compared between groups to reveal local surface deformations/expansions and the results were displayed on the group averaged left or right amygdala.

STATISTICAL ANALYSES

Analyses of the amygdala volumes were conducted using SPSS (SPSS Inc, Chicago, Illinois). The general linear model was used to assess the amygdala volume differences between the psychopathy and control groups, while covarying for total brain volume. Socioeconomic status and substance dependence, for which groups differed significantly, were also included in the statistical analyses as covariates. Partial correlations were conducted on the entire sample of 59 to assess the association between amygdala volume and total and facet psychopathy scores, while controlling for total brain volume. All tests of significance were 2-tailed with an α level of .05.

The same statistical models described earlier were implemented using the statistical program R (www.r-project.org) to identify regional changes in amygdala surface anatomy between groups and assess relationships between amygdala surface deformations and psychopathy scores. Uncorrected 2-tailed probability values obtained from these analyses conducted for each amygdala surface point were color coded and displayed on the averaged surface of the entire group to allow initial visualization of localized group differences in amygdala surface structure. Structural variation of the human amygdala and individual differences in the relative position of amygdala nuclei across the surface do not allow the locations of amygdala nuclei to be determined with a high degree of accuracy in imaging data. Thus, the boundaries of the different subnuclei (Figure 2) are approximations as they are based on an extrapolation of the relative nuclei positions in 1 atlas.53 Permutation tests with a threshold of P < .05 were applied to control for multiple spatially correlated comparisons (statistical tests performed at 15 000 amygdala surface locations) to ensure that the overall pattern of effects in the surface-based maps could not have been observed by chance alone.5658

RESULTS
PSYCHOPATHIC INDIVIDUALS VS CONTROLS
Subject Characteristics

Groups differed significantly on socioeconomic status and history of substance/alcohol dependence (Table 1). To rule out these potential confounds, they were included as covariates in the general linear models used for the volumetric analyses as well as the surface-based analyses.

Traditional Volumetric Analyses

Psychopathic individuals showed a significant volume reduction in the amygdala compared with controls (F2,55 = 3.85; P = .03), with whole-brain volume as a covariate. As illustrated in Figure 3, individuals with psychopathy showed a 17.14% volume reduction in the left amygdala and an 18.93% volume reduction in the right amygdala compared with controls. While the right amygdala showed a tendency toward greater volumetric reduction than the left, no significant laterality effect was observed (F1,56 = 0.61; P = .44). Group differences for both left and right amygdala volumes remained significant after correcting for the whole-brain volume, socioeconomic status, and substance/alcohol dependence (P = .02 and P = .02, respectively).

Surface-Based Mesh Modeling Methods

Surface-based modeling analysis revealed bilateral shape differences of the amygdala that were consistent with the volumetric findings (left, permutation-corrected P = .047; right, P = .002) (Figure 2). The results remained significant after controlling for whole-brain volume, socioeconomic status, and substance/alcohol dependence (left, permutation-corrected P = .049; right, P = .006). In terms of localization, little evidence could be found for deformations in the vicinity of accessory basal nuclei, basomedial nuclei, medial amygdaloid nuclei, and piriform cortex (Figure 2). Regarding the remaining 9 nuclei, the strongest evidence was found for deformations in the approximate locations of anterior and posterior cortical and central nuclei (superior view) and basolateral and lateral nuclei (superior and inferior view) of the amygdala.

CORRELATION ANALYSES
Traditional Volumetric Analyses

To determine whether the amygdala volume deficit was associated with a particular facet of psychopathy, correlational analyses on the entire sample of 59 subjects were conducted. Findings revealed significant negative correlations between amygdala volumes and the psychopathy total and facet scores, with the correlations strongest for the affective and interpersonal facets (Table 2). All findings remained significant after controlling for whole-brain volume, socioeconomic status, and substance/alcohol dependence (all P < .01).

Surface-Based Mesh Modeling Methods

As demonstrated in Figure 4, surface-based analyses revealed similar negative correlations between the amygdala and psychopathy scores, which again were more pronounced for the affective and interpersonal facets. The permutation analyses showed that bilateral amygdala deformations were significantly correlated with total (left, permutation-corrected P = .004; right, P < .001), interpersonal (left, permutation-corrected P < .001; right, P = .001), and affective (left, permutation-corrected P < .001; right, P < .001) scores. The lifestyle and antisocial facets of psychopathy showed significant associations with the left amygdala (permutation-corrected P = .02 and .01, respectively) but not the right amygdala (permutation-corrected P = .12 and .16, respectively). These correlations remained significant after controlling for whole-brain volume, socioeconomic status, and substance/alcohol dependence (all permutation-corrected P < .03). Consistent with group analyses, increased psychopathy scores were associated with increased regional atrophy approximately in the cortical, central, basolateral, and lateral nuclei of the amygdala (Figure 4).

COMMENT

To our knowledge, this study is the first to show localized structural abnormalities of the amygdala in individuals with psychopathy. In this study, psychopathic individuals were found to show bilateral amygdala volume reductions compared with controls. Significant regional deformations were found to be most prominent in the vicinity of the basolateral, lateral, cortical, and central nuclei of the amygdala in individuals with psychopathy. In addition, negative correlations were found between amygdala volumes and all 4 psychopathy facet scores, with correlations being most pronounced for the affective and interpersonal facets of psychopathy. Results could not be attributed to demographic group differences in socioeconomic status or substance/alcohol dependence. Findings provide initial evidence indicating amygdala structural abnormalities as 1 key element in the neurobiological bases of psychopathy.

Findings of amygdala volume reductions in individuals with psychopathy are consistent with lesion studies showing that damage to the amygdala results in emotional impairments similar to those of psychopathy. Animals with selective lesions to the amygdala have been found to show substantial impairments in fear conditioning and abnormal responsivity to threatening objects. For example, Hitchcock and Davis59 demonstrated that lesions to the amygdala impaired fear-potentiated startle response in rats. In a recent study, Machado and Bachevalier60 found that rhesus monkeys with selective lesions to the amygdala showed profound behavioral changes that precluded positive social interactions (eg, decreased affiliation and popularity within the group) and decreased reactivity to threatening gestures. Similar findings have been reported showing that monkeys with bilateral amygdala lesions displayed blunted emotional response (ie, lack of fear) and decreased defensive behavior to threats (ie, a fake snake).61,62 These behavioral changes found in animals with amygdala lesions may suggest, albeit indirectly, that amygdala structural abnormalities may contribute to the classic findings of poor fear conditioning and impaired emotion recognition observed in individuals with psychopathy.7,9,63

In humans, selective lesions to the amygdala are rare, making it difficult to draw clear conclusions regarding the role such lesions play in modulating the emotion and behavior of patients. However, evidence suggests that there are similarities between the affective and social impairments resulting from amygdala lesions and the behavioral dysfunctions characterizing individuals with psychopathy. For example, Adolphs et al19 demonstrated in a case study that extensive bilateral amygdala damage (as a result of Urbach-Wiethe disease) led to difficulty in recognizing emotions in facial expressions, particularly when the patient was responding to a highly arousing facial expression such as fear, similar to the impairments observed in individuals with psychopathy.64 Several subsequent studies reported similar findings and show a consistent pattern of intact facial identification and impaired recognition of the facial expression of fear in patients with amygdala lesions such as those caused by disease (eg, encephalitis) and/or resection (eg, lobectomy or amygdalotomy).15,6571

Observations from studies of patients with temporal lobe epilepsy (TLE) may also provide evidence in support of our findings linking altered amygdala morphology with psychopathy. Although amygdala damage in patients with TLE often occurs in conjunction with damage to other regions of the brain, pathological findings are regionally isolated in some cases.7274 Volumetric reductions indicating pathology of the amygdala are frequently documented in patients with TLE (with reports ranging between 10%-57% amygdala volume reductions),75 where the lateral and basal nuclei appear most susceptible to seizure-induced damage.72,7577 Patients who have TLE and exhibit concomitant amygdala damage have been found to show impairments in emotion recognition. For example, Houghton et al78 reported that impairments in the ability to recognize negative emotional expressions were associated with reduced amygdala volume in patients with TLE. In addition, several studies have shown that TLE-induced amygdala damage also results in impaired social judgment (ie, rate aversive facial appearances as more positive) because of the difficulty in recognizing negative facial emotions,79,80 again consistent with behavioral dysfunction reported in individuals with psychopathy. These human lesion studies demonstrate that amygdala lesions lead to outcomes of affective impairments that parallel to some extent the profile of individuals with psychopathy7,12,81 and support the findings of this study in suggesting that structural impairments in the amygdala may predispose to the emotional and social dysfunction in individuals with psychopathy.

The surface-based mesh modeling analyses indicate regional atrophy in amygdala structure in the vicinity of the basolateral, lateral, central, and cortical nuclei in individuals with psychopathy, echoing the complexity of the clinical descriptions of this disorder. The most robust evidence suggests that the lateral, basolateral, and central nuclei of the amygdala are independently and interactively involved in emotional processing, including fear conditioning and autonomic reactivity to affective stimuli,2830 while other studies have further linked these nuclei to reward-related learning, behavioral inhibition, and decision making.28 With regard to the cortical nuclei, the very few findings are suggestive that this region may be involved in parenting, social interaction, and the regulation of stress and anxiety.28 Therefore, the regional morphological abnormalities of the amygdala observed in this study may reflect a variety of emotional and behavioral features in individuals with psychopathy. Future research using higher-resolution imaging will be needed to identify the structural alterations within each nucleus of the amygdala, but the even greater challenge will be to delineate the human functional significance of such deformations based on the behavioral neuroscience animal literature.

In addition to the significant amygdala volume reductions in individuals with psychopathy, reduced volumes were found to correlate with increased total psychopathy scores across the entire sample. The correlations were found to be most pronounced for the affective and interpersonal facets of psychopathy. These findings are consistent with 1 abstract reporting a correlation between reduced volumes in the right amygdala and increased affective-interpersonal scores of psychopathy in a violent offender sample.82 Results are further supported by evidence from functional imaging studies showing a higher degree of abnormal activation in the amygdala to be associated with an increase in the psychopathy score during affect recognition, prisoner's dilemma tasks, and moral decision making.8385 The associations between reduced amygdala volume and increased psychopathy total and facet scores are in line with evidence indicating that, in addition to emotional processing, the amygdala mediates a variety of brain functions, including attention, memory, social judgment, and moral decision making, through its neural connections with the prefrontal cortex and other subcortical structures.79,8689 Therefore, our findings support the hypothesis that a higher degree of structural abnormalities in the amygdala may contribute to a greater manifestation of the affective-interpersonal impairments and, to a lesser degree, an increase in antisocial behavior and lifestyle in individuals with psychopathy.

There are several potential limitations of the present study that need to be taken into account when interpreting the results. First, the sample size is modest, thus raising the risk of potential type II error. However, the sample size is comparable with those used in other magnetic resonance imaging studies, and the use of correlation analyses on the entire sample of 59 subjects increases the power for detecting any association between amygdala volume and psychopathy. Second, there was the lack of absolute objectivity due to the nature of manual tracing. However, the method was used to test the specific hypotheses of regional morphological deformations in the amygdala in individuals with psychopathy, which would not have been possible if an automated imaging analysis method, such as voxel-based morphometry, was used. Third, although we controlled for socioeconomic status and substance dependence, a possibility remains that other confounds may contribute to the amygdala structural alterations observed in individuals with psychopathy, such as pharmacological treatments received prior to the scanning. Another limitation of this study is that even though we were able to conduct the group comparisons on a surface point-by-point level to elucidate the approximate locations of the amygdala deformations, we were unable to test the significance values for each distinct nucleus. Therefore, while surface maps indicate a more pronounced amygdala deformation in the cortical, central, basolateral, and lateral nuclei, the possibility remains that the findings also reflect deformations of nuclei relatively less represented on the surface (eg, medial amygdaloid and basomedial nuclei). Last, the standard resolution of structural imaging data does not yet allow reliable localization of structural alterations within specific amygdala nuclei. The precise identification of the amygdala nuclei in humans requires a combination of histological/immunohistochemical methods and neurochemical and cytoarchitectonic criteria,90 which was not possible in this study using in vivo imaging with a 1.5-T scanner. As a result, it needs to be made clear that the labeling of the schematic representation of the amygdala nuclei shown in this study was based on information obtained from a single human brain atlas53 and has not been validated in any probabilistic manner. Nonetheless, this approach was chosen taking into account the methodological and technological difficulties to best illustrate the approximate locations of regional amygdala deformations in individuals with psychopathy and illuminate the need for future studies to examine the amygdala as a heterogeneous structure and identify subtle and localized structural changes within the amygdala. Although the precise localization of structural changes within specific nuclei awaits further research, this study is the first, to our knowledge, to provide an examination of localized morphological alterations in the amygdala in individuals with psychopathy. The advance in the understanding of the neuropathology in psychopathy could greatly benefit from future studies examining the mediating risk factors (eg, autonomic fear conditioning response) together with structural imaging data to translate amygdala structural impairments directly into functional impairments in individuals with psychopathy.

CONCLUSIONS

It is increasingly argued that deficits in the amygdala may be a crucial component in the neurobiological mechanisms underlying psychopathy.3134 The findings in this study provide the first evidence, to our knowledge, showing significant volume reductions and regional morphological alterations in bilateral amygdala in psychopathic individuals and indicate that structural impairments are most prominent in the vicinity of basolateral, lateral, central, and cortical nuclei. The amygdala reductions may particularly predispose to core psychopathic features of emotional and social dysfunctions. Although future prospective longitudinal research is required to determine the neural mechanisms in psychopathy, this study highlights the importance of the amygdala as a potentially critical neural substrate for both emotional and behavioral features of psychopathy.

Back to top
Article Information

Correspondence: Yaling Yang, PhD, Laboratory of Neuro Imaging, Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90095 (yaling.yang@loni.ucla.edu).

Submitted for Publication: August 27, 2008; final revision received February 11, 2009; accepted February 15, 2009.

Financial Disclosure: None reported.

Funding/Support: This study was supported by National Research Service Award 1F31MH079592 (Dr Yang), grants K02 MH01114-06 and MH50940 (Dr Raine), and Career Development Award K01 MH073990 from the National Institute of Mental Health, research grant P41 RR13642 from the National Center for Research Resources, and grant U54 RR021813 from the National Institutes of Health through the NIH Roadmap for Medical Research.

Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health or the National Institutes of Health.

Additional Contributions: Shannon Bell, BA, Sheri Leung, BA, and Owen Phillips, BS, assisted with data scoring and analysis.

References
1.
Cleckley  H The Mask of Sanity.  St Louis, MO Mosby1941;
2.
Cooke  DJMichie  CHart  SD Facets of clinical psychopathy: toward clearer measurement. Patrick  CJHandbook of Psychopathy. New York, NY The Guilford Press2005;
3.
Hare  RD Manual for the Hare Psychopathy Checklist–Revised.  Toronto, ON, Canada Multi-Health Systems1991;
4.
Patrick  CJ Emotional processes in psychopathy. Raine  ASanmartín  JViolence and Psychopathy. New York, NY Kluwer Academic/Plenum Publishers2001;
5.
Arnett  PA Autonomic responsivity in psychopaths: a critical review and theoretical proposal. Clin Psychol Rev 1997;17 (8) 903- 936
PubMedArticle
6.
Kiehl  KAHare  RD McDonald  JJBrink  J Semantic and affective processing in psychopaths: an event-related potential (ERP) study. Psychophysiology 1999;36 (6) 765- 774
PubMedArticle
7.
Patrick  CJBradley  MMLang  PJ Emotion in the criminal psychopath: startle reflex modulation. J Abnorm Psychol 1993;102 (1) 82- 92
PubMedArticle
8.
Raine  A Evoked potentials and psychopathy. Int J Psychophysiol 1989;8 (1) 1- 16
PubMedArticle
9.
Raine  A Crime, conditioning, and arousal. Nyborg  HThe Scientific Study of Human Nature Tribute to Hanes J. Eysenck. Oxford, England: Elsevier1997;
10.
Stanford  MSHouston  RJBarratt  ES Psychophysiological correlates of psychopathic disorders. Felthous  ARSaß  HInternational Handbook on Psychopathic Disorders and the Law. Hoboken, NJ John Wiley & Sons Inc2007;
11.
Patrick  CJ Emotion and psychopathy: startling new insights. Psychophysiology 1994;31 (4) 319- 330
PubMedArticle
12.
Patrick  CJCuthbert  BNLang  PJ Emotion in the criminal psychopath: fear image processing. J Abnorm Psychol 1994;103 (3) 523- 534
PubMedArticle
13.
Williamson  SHarpur  TJHare  RD Abnormal processing of affective words by psychopaths. Psychophysiology 1991;28 (3) 260- 273
PubMedArticle
14.
Adolphs  RTranel  DDamasio  HDamasio  AR Fear and the human amygdala. J Neurosci 1995;15 (9) 5879- 5891
PubMed
15.
Adolphs  RTranel  DHamann  SYoung  AWCalder  AJPhelps  EAAnderson  ALee  GPDamasio  AR Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 1999;37 (10) 1111- 1117
PubMedArticle
16.
Brothers  LRing  BKling  A Response of neurons in the macaque amygdala to complex social stimuli. Behav Brain Res 1990;41 (3) 199- 213
PubMedArticle
17.
Kling  AGreen  PC Effects of neonatal amygdalectomy in the maternally reared and maternally deprived monkey. Nature 1967;213 (5077) 742- 743
PubMedArticle
18.
Phelps  EA Emotion and cognition: insights from studies of the human amygdala. Annu Rev Psychol 2006;5727- 53
PubMedArticle
19.
Adolphs  RTranel  DDamasio  HDamasio  A Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 1994;372 (6507) 669- 672
PubMedArticle
20.
Blair  RJ The roles of orbitofrontal cortex in the modulation of antisocial behavior. Brain Cogn 2004;55 (1) 198- 208
PubMedArticle
21.
Baxter  MGMurray  EA The amygdala and reward. Nat Rev Neurosci 2002;3 (7) 563- 573
PubMedArticle
22.
Blair  RJR The amygdala and ventromedial prefrontal cortex in morality and psychopathy. Trends Cogn Sci 2007;11 (9) 387- 392
PubMedArticle
23.
Davis  M The role of the amygdala in conditioned fear. Aggleton  JPThe Amygdala Neurobiological Aspects of Emotion, Memory and Mental Dysfunction. New York, NY: Wiley-Liss1992;
24.
Everitt  BJCardinal  RNParkinson  JARobbins  TW Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning. Ann N Y Acad Sci 2003;985233- 250
PubMedArticle
25.
Holland  PCGallagher  M Amygdala-frontal interactions and reward expectancy. Curr Opin Neurobiol 2004;14 (2) 148- 155
PubMedArticle
26.
LeDoux  JE The Emotional Brain.  New York, NY Simon & Schuster1996;
27.
Raine  AYang  Y Neural foundations to moral reasoning and antisocial behavior. Soc Cogn Affect Neurosci 2006;1 (3) 203- 213
PubMedArticle
28.
Knapska  ERadwanska  KWerka  TKaczmarek  L Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. Physiol Rev 2007;87 (4) 1113- 1173
PubMedArticle
29.
Sah  PFaber  ESLopez De Armentia  MPower  J The amygdaloid complex: anatomy and physiology. Physiol Rev 2003;83 (3) 803- 834
PubMed
30.
Balleine  BWKillcross  S Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci 2006;29 (5) 272- 279
PubMedArticle
31.
Blair  RJJones  LClark  FSmith  M The psychopathic individual: a lack of responsiveness to distress cues? Psychophysiology 1997;34 (2) 192- 198
PubMedArticle
32.
Damasio  A Descartes' Error: Emotion, Reason, and the Human Brain.  New York, NY GP Putnam's Sons1994;
33.
Kiehl  KA A cognitive neuroscience perspective on psychopathy: evidence for paralimbic system dysfunction. Psychiatry Res 2006;142 (2-3) 107- 128
PubMedArticle
34.
Yang  YRaine  A Functional and structural brain imaging research on psychopathy. Felthous  AHSass  HInternational Handbook on Psychopathic Disorders and the Law. Hoboken, NJ Wiley2006;
35.
Hare  RD Manual for the Revised Psychopathy Checklist. 2nd ed. Toronto, ON, Canada Multi-Health Systems2003;
36.
Raine  ALencz  TBihrle  SLaCasse  LColletti  P Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. Arch Gen Psychiatry 2000;57 (2) 119- 127, discussion 128-129
PubMedArticle
37.
Kosson  DSSteuerwald  BLForth  AEKirkhart  KJ A new method for assessing the interpersonal behavior of psychopathic individuals: preliminary validation studies. Psychol Assess 1997;9 (2) 89- 101Article
38.
Elliott  DSAgeton  SSHuizinga  DKnowles  BACanter  RJ The Prevalence and Incidence of Delinquent Behavior: 1976-1980—National Estimates of Delinquent Behavior by Sex, Race, Social Class and Other Selected Variables.  Boulder, CO Behavior Research Institute1983;National Youth Survey Report No. 26
39.
First  MBSpitzer  RLGibbon  MWilliams  JBW Structured Clinical Interview for Axis I DSM-IV Disorders (SCID, Version 2.0).  New York New York State Psychiatric Institute1994;
40.
First  MBSpitzer  RLGibbon  MWilliams  JBWBenjamin  L Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II, Version 2.0).  New York New York State Psychiatric Institute1994;
41.
Yang  YRaine  ALencz  TBihrle  SLaCasse  LColletti  P Volume reduction in prefrontal gray matter in unsuccessful criminal psychopaths. Biol Psychiatry 2005;57 (10) 1103- 1108
PubMedArticle
42.
Raine  AIshikawa  SSArce  ELencz  TKnuth  KHBihrle  SLaCasse  LColletti  P Hippocampal structural asymmetry in unsuccessful psychopaths. Biol Psychiatry 2004;55 (2) 185- 191
PubMedArticle
43.
Raine  ALencz  TTaylor  KHellige  JBBihrle  SLacasse  LLee  MIshikawa  SColletti  P Corpus callosum abnormalities in psychopathic antisocial individuals. Arch Gen Psychiatry 2003;60 (11) 1134- 1142
PubMedArticle
44.
Harris  GTRice  MEQuinsey  VL Psychopathy as a taxon: evidence that psychopaths are a discrete class. J Consult Clin Psychol 1994;62 (2) 387- 397
PubMedArticle
45.
Hollingshead  AB Four Factor Index of Social Status.  New Haven, CT Department of Sociology, Yale University1975;
46.
Wechsler  D Wechsler Adult Intelligence Scale–Revised.  San Antonio, TX Psychological Corp1981;
47.
Bryden  MP Measuring handedness with questionnaires. Neuropsychologia 1977;15 (4-5) 617- 624
PubMedArticle
48.
Sled  JGPike  GB Standing-wave and RF penetration artifacts caused by elliptic geometry: an electrodynamic analysis of MRI. IEEE Trans Med Imaging 1998;17 (4) 653- 662
PubMedArticle
49.
Mazziotta  JCToga  AWEvans  AFox  PLancaster  JThe International Consortium for Brain Mapping (ICBM), A probabilistic atlas of the human brain: theory and rationale for its development. Neuroimage 1995;2 (2) 89- 101
PubMedArticle
50.
Narr  KLThompson  PMSharma  TMoussai  JBlanton  RAnvar  BEdris  AKrupp  RRayman  JKhaledy  MToga  AW Three-dimensional mapping of temporo-limbic regions and the lateral ventricles in schizophrenia: gender effects. Biol Psychiatry 2001;50 (2) 84- 97
PubMedArticle
51.
Bartzokis  GMintz  JMarx  POsborn  DGutkind  DChiang  FPhelan  CKMarder  SR Reliability of in vivo volume measures of hippocampus and other brain structures using MRI. Magn Reson Imaging 1993;11 (7) 993- 1006
PubMedArticle
52.
Levitt  JGBlanton  RECaplan  RAsarnow  RGuthrie  DToga  AWCapetillo-Cunliffe  L McCracken  JT Medial temporal lobe in childhood-onset schizophrenia. Psychiatry Res 2001;108 (1) 17- 27
PubMedArticle
53.
Mai  JKAssheuer  JPaxinos  G Atlas of the Human Brain.  San Diego, CA Academic Press1997;
54.
Yang  YRaine  ANarr  KLLencz  TLaCasse  LColletti  PToga  AW Localisation of increased prefrontal white matter in pathological liars. Br J Psychiatry 2007;190174- 175
PubMedArticle
55.
Ballmaier  MNarr  KLToga  AWElderkin-Thompson  VThompson  PMHamilton  LHaroon  EPham  DHeinz  AKumar  A Hippocampal morphology and distinguishing late-onset from early-onset elderly depression. Am J Psychiatry 2008;165 (2) 229- 237
PubMedArticle
56.
Narr  KLThompson  PMSzeszko  PRobinson  DJang  SWoods  RPKim  SHayashi  KMAsunction  DToga  AWBilder  RM Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage 2004;21 (4) 1563- 1575
PubMedArticle
57.
Thompson  PMHayashi  KMDe Zubicaray  GLJanke  ALRose  SESemple  JHong  MSHerman  DHGravano  DDoddrell  DMToga  AW Mapping hippocampal and ventricular change in Alzheimer's disease. Neuroimage 2004;22 (4) 1754- 1766
PubMedArticle
58.
Bullmore  ETSuckling  JOvermeyer  SRabe-Hesketh  STaylor  EBrammer  MJ Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 1999;18 (1) 32- 42
PubMedArticle
59.
Hitchcock  JDavis  M Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav Neurosci 1986;100 (1) 11- 22
PubMedArticle
60.
Machado  CJBachevalier  J The impact of selective amygdala, orbitofrontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behav Neurosci 2006;120 (4) 761- 786
PubMedArticle
61.
Kalin  NHShelton  SEDavidson  RJKelley  AE The primate amygdala mediates acute fear but not the behavioral physiological components of anxious temperament. J Neurosci 2001;21 (6) 2067- 2074
PubMed
62.
Izquierdo  ASuda  RKMurray  EA Comparison of the effects of bilateral orbital prefrontal cortex lesions and amygdala lesions on emotional responses in rhesus monkeys. J Neurosci 2005;25 (37) 8534- 8542
PubMedArticle
63.
Hare  HD Electrodermal and cardiovascular correlates of psychopathy. Hare  RDSchalling  DPsychopathic Behavioral Approaches to Research. New York, NY: Wiley1978;
64.
Marsh  AABlair  RJ Deficits in facial affect recognition among antisocial populations: a meta-analysis. Neurosci Biobehav Rev 2008;32 (3) 454- 465
PubMedArticle
65.
Adolphs  RBaron-Cohen  STranel  D Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci 2002;14 (8) 1264- 1274
PubMedArticle
66.
Anderson  AKSpencer  DDFulbright  RKPhelps  EA Contribution of the anteromedial temporal lobes to the evaluation of facial emotion. Neuropsychology 2000;14 (4) 526- 536
PubMedArticle
67.
Anderson  AKPhelps  EA Intact recognition of vocal expressions of fear following bilateral lesions of the human amygdala. Neuroreport 1998;9 (16) 3607- 3613
PubMedArticle
68.
Anderson  AKPhelps  EA Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 2001;411 (6835) 305- 309
PubMedArticle
69.
Broks  PYoung  AWMaratos  EJCoffey  PJCalder  AJIsaac  CLMayes  ARHodges  JRMontaldi  DCezayirli  ERoberts  NHadley  D Face processing impairments after encephalitis: amygdala damage and recognition of fear. Neuropsychologia 1998;36 (1) 59- 70
PubMedArticle
70.
Young  AWHellawell  DJVan De Wal  CJohnson  M Facial expression processing after amygdalotomy. Neuropsychologia 1996;34 (1) 31- 39
PubMedArticle
71.
Schmolck  HSquire  LR Impaired perception of facial emotions following bilateral damage to the anterior temporal lobe. Neuropsychology 2001;15 (1) 30- 38
PubMedArticle
72.
Hudson  LPMunoz  DGMiller  L McLachlan  RSGirvin  JPBlume  WT Amygdaloid sclerosis in temporal lobe epilepsy. Ann Neurol 1993;33 (6) 622- 631
PubMedArticle
73.
Miller  LA McLachlan  RSBouwer  MSHudson  LPMunoz  DG Amygdalar sclerosis: preoperative indicators and outcome after temporal lobectomy. J Neurol Neurosurg Psychiatry 1994;57 (9) 1099- 1105
PubMedArticle
74.
Guerreiro  CCendes  FLi  LMJones-Gotman  MAndermann  FDubeau  FPiazzini  AFeindel  W Clinical patterns of patients with temporal lobe epilepsy and pure amygdalar atrophy. Epilepsia 1999;40 (4) 453- 461
PubMedArticle
75.
Pitkänen  ATuunanen  JKälviäinen  RPartanen  KSalmenperä  T Amygdala damage in experimental and human temporal lobe epilepsy. Epilepsy Res 1998;32 (1-2) 233- 253
PubMedArticle
76.
Meyer  ABeck  EShepherd  M Unusually severe lesions in the brain following status epilepticus. J Neurol Neurosurg Psychiatry 1955;18 (1) 24- 33
PubMedArticle
77.
Margerison  JHCorsellis  JA Epilepsy and the temporal lobes: a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 1966;89 (3) 499- 530
PubMedArticle
78.
Houghton  JMBroks  PWing  AEldridge  PWalsh  RDavies  PJukes  RKuczynski  AReynders  H Does temporal lobe epilepsy impair the ability to recognize cues to the emotional state of others? Epilepsia 2000;41 ((suppl 7)) 249
79.
Adolphs  RTranel  DDamasio  AR The human amygdala in social judgment. Nature 1998;393 (6684) 470- 474
PubMedArticle
80.
Reynders  HJBroks  PDickson  JMLee  CETurpin  G Investigation of social and emotion information processing in temporal lobe epilepsy with ictal fear. Epilepsy Behav 2005;7 (3) 419- 429
PubMedArticle
81.
Plutchik  R Emotions and sociopathy. Behav Brain Sci 1995;18 (3) 570- 571Article
82.
Tiihonen  JHodgins  SVaurio  O Amygdaloid volume loss in psychopathy. Abstr Soc Neurosci 2000;2017
83.
Gordon  HLBaird  AAEnd  A Functional differences among those high and low on a trait measure of psychopathy. Biol Psychiatry 2004;56 (7) 516- 521
PubMedArticle
84.
Rilling  JKGlenn  ALJairam  MRPagnoni  GGoldsmith  DRElfenbein  HALilienfeld  SO Neural correlates of social cooperation and non-cooperation as a function of psychopathy. Biol Psychiatry 2007;61 (11) 1260- 1271
PubMedArticle
85.
Glenn  ALRaine  ASchug  RA The neural correlates of moral decision-making in psychopathy. Mol Psychiatry 2009;14 (1) 5- 6
PubMedArticle
86.
Anderson  AKPhelps  EA Expression without recognition: contributions of the human amygdala to emotional communication. Psychol Sci 2000;11 (2) 106- 111
PubMedArticle
87.
McGaugh  JL The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 2004;271- 28
PubMedArticle
88.
Sarter  MMarkowitsch  HJ Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations. Behav Neurosci 1985;99 (2) 342- 380
PubMedArticle
89.
Whalen  PJ The uncertainty of it all. Trends Cogn Sci 2007;11 (12) 499- 500
PubMedArticle
90.
Savander  VGo  CLedoux  JEPitkänen  A Intrinsic connections of the rat amygdaloid complex: projections originating in the basal nucleus. J Comp Neurol 1995;361 (2) 345- 368
PubMedArticle
×