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Amygdala and Orbitofrontal Reactivity to Social Threat in Individuals with Impulsive Aggression

  • Emil F. Coccaro
    Correspondence
    Address reprint requests to Emil F. Coccaro, M.D., Department of Psychiatry, The University of Chicago, 5841 South Maryland Avenue MC3077, Chicago, IL 60637-1470
    Affiliations
    Department of Psychiatry, Biological Sciences Division and the Pritzker School of Medicine, The University of Chicago, Chicago, Illinois

    Center for Cognitive and Social Neuroscience, The University of Chicago, Chicago, Illinois.
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  • Michael S. McCloskey
    Affiliations
    Department of Psychiatry, Biological Sciences Division and the Pritzker School of Medicine, The University of Chicago, Chicago, Illinois

    Center for Cognitive and Social Neuroscience, The University of Chicago, Chicago, Illinois.
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  • Daniel A. Fitzgerald
    Affiliations
    Department of Psychiatry, Biological Sciences Division and the Pritzker School of Medicine, The University of Chicago, Chicago, Illinois
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  • K. Luan Phan
    Affiliations
    Department of Psychiatry, Biological Sciences Division and the Pritzker School of Medicine, The University of Chicago, Chicago, Illinois

    Center for Cognitive and Social Neuroscience, The University of Chicago, Chicago, Illinois.
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      Background

      Converging evidence from animal and human lesion studies implicates the amygdala and orbitofrontal cortex (OFC) in emotional regulation and aggressive behavior. However, it remains unknown if functional deficits exist in these specific brain regions in clinical populations in which the cardinal symptom is impulsive aggression. We have previously shown that subjects diagnosed with intermittent explosive disorder (IED), a psychiatric disorder characterized by reactive aggressive behavior, perform poorly on facial emotion recognition tasks. In this study we employed a social-emotional probe of amygdala-OFC function in individuals with impulsive aggression.

      Methods

      Ten unmedicated subjects with IED and 10 healthy, matched comparison subjects (HC) underwent functional magnetic resonance imaging while viewing blocks of emotionally salient faces. We compared amygdala and OFC reactivity to faces between IED and HC subjects, and examined the relationship between the extent of activation in these regions and extent of prior history of aggressive behavior.

      Results

      Relative to controls, individuals with IED exhibited exaggerated amygdala reactivity and diminished OFC activation to faces expressing anger. Extent of amygdala and OFC activation to angry faces were differentially related to prior aggressive behavior across subjects. Unlike controls, aggressive subjects failed to demonstrate amygdala-OFC coupling during responses to angry faces.

      Conclusions

      These findings provide evidence of amygdala-OFC dysfunction in response to an ecologically-valid social threat signal (processing angry faces) in individuals with a history of impulsive aggressive behavior, and further substantiate a link between a dysfunctional cortico-limbic network and aggression.

      Key Words

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      References

        • Adamec R.E.
        Partial kindling of the ventral hippocampus: identification of changes in limbic physiology which accompany changes in feline aggression and defense.
        Physiol Behav. 1991; 49: 443-453
        • Adams Jr, R.B.
        • Gordon H.L.
        • Baird A.A.
        • Ambady N.
        • Kleck R.E.
        Effects of gaze on amygdala sensitivity to anger and fear faces.
        Science. 2003; 300: 1536
        • Adolphs R.
        Neural systems for recognizing emotion.
        Curr Opin Neurobiol. 2002; 12: 169-177
        • Adolphs R.
        • Baron-Cohen S.
        • Tranel D.
        Impaired recognition of social emotions following amygdala damage.
        J Cogn Neurosci. 2002; 14: 1264-1274
        • Adolphs R.
        • Gosselin F.
        • Buchanan T.W.
        • Tranel D.
        • Schyns P.
        • Damasio A.R.
        A mechanism for impaired fear recognition after amygdala damage.
        Nature. 2005; 433: 68-72
        • Amaral D.G.
        • Bauman M.D.
        • Capitanio J.P.
        • Lavenex P.
        • Mason W.A.
        • Mauldin-Jourdain M.L.
        • Mendoza S.P.
        The amygdala: is it an essential component of the neural network for social cognition?.
        Neuropsychologia. 2003; 41: 517-522
        • Amaral D.G.
        • Price J.L.
        Amygdalo-cortical projections in the monkey (Macaca fascicularis).
        J Comp Neurol. 1984; 230: 465-496
        • American Psychiatric Association
        Diagnostic and statistical manual of mental disorders: DSM-IV-TR. 4th ed. American Psychiatric Association, Washington, DC2000
        • Anderson S.W.
        • Bechara A.
        • Damasio H.
        • Tranel D.
        • Damasio A.R.
        Impairment of social and moral behavior related to early damage in human prefrontal cortex.
        Nat Neurosci. 1999; 2: 1032-1037
        • Beck A.T.
        • Ward C.H.
        • Mendelson M.
        • Mock J.
        • Erbaugh J.
        An inventory for measuring depression.
        Arch Gen Psychiatry. 1961; 4: 561-571
        • Beer J.S.
        • Heerey E.A.
        • Keltner D.
        • Scabini D.
        • Knight R.T.
        The regulatory function of self-conscious emotion: insights from patients with orbitofrontal damage.
        J Pers Soc Psychol. 2003; 85: 594-604
        • Best M.
        • Williams J.M.
        • Coccaro E.F.
        Evidence for a dysfunctional prefrontal circuit in patients with an impulsive aggressive disorder.
        Proc Natl Acad Sci USA. 2002; 99: 8448-8453
        • Birbaumer N.
        • Veit R.
        • Lotze M.
        • Erb M.
        • Hermann C.
        • Grodd W.
        • Flor H.
        Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study.
        Arch Gen Psychiatry. 2005; 62: 799-805
        • Blair R.J.
        Neurobiological basis of psychopathy.
        Br J Psychiatry. 2003; 182: 5-7
        • Blair R.J.
        • Morris J.S.
        • Frith C.D.
        • Perrett D.I.
        • Dolan R.J.
        Dissociable neural responses to facial expressions of sadness and anger.
        Brain. 1999; 122: 883-893
        • Blair R.J.
        • Peschardt K.S.
        • Budhani S.
        • Mitchell D.G.
        • Pine D.S.
        The development of psychopathy.
        J Child Psychol Psychiatry. 2006; 47: 262-276
        • Buss A.H.
        • Perry M.
        The aggression questionnaire.
        J Pers Soc Psychol. 1992; 63: 452-459
        • Cavada C.
        • Company T.
        • Tejedor J.
        • Cruz-Rizzolo R.J.
        • Reinoso-Suarez F.
        The anatomical connections of the macaque monkey orbitofrontal cortex.
        Cereb Cortex. 2000; 10: 220-242
        • Coccaro E.F.
        Central serotonin and impulsive aggression.
        Br J Psychiatry Suppl. 1989; : 52-62
        • Coccaro E.F.
        Intermittent explosive disorder. Marcel Dekker Inc, New York2003
        • Coccaro E.F.
        Intermittent explosive disorder.
        in: Coccaro E.F. Aggression: Psychiatric Assessment and Treatment. 2003: 149-199
        • Coccaro E.F.
        • Berman M.E.
        • Kavoussi R.J.
        Assessment of life history of aggression: development and psychometric characteristics.
        Psychiatry Res. 1997; 73: 147-157
        • Coccaro E.F.
        • Kavoussi R.J.
        Fluoxetine and impulsive aggressive behavior in personality-disordered subjects.
        Arch Gen Psychiatry. 1997; 54: 1081-1088
        • Coccaro E.F.
        • Kavoussi R.J.
        • Berman M.E.
        • Lish J.D.
        Intermittent explosive disorder-revised: development, reliability, and validity of research criteria.
        Compr Psychiatry. 1998; 39: 368-376
        • Coccaro E.F.
        • Schmidt C.A.
        • Samuels J.F.
        • Nestadt G.
        Lifetime and 1-month prevalence rates of intermittent explosive disorder in a community sample.
        J Clin Psychiatry. 2004; 65: 820-824
        • Crick N.R.
        • Dodge K.A.
        Social information-processing mechanisms in reactive and proactive aggression.
        Child Dev. 1996; 67: 993-1002
        • Damasio A.R.
        Descartes’ Error. Avon Books, Inc, New York1994
        • Damasio A.R.
        • Grabowski T.J.
        • Bechara A.
        • Damasio H.
        • Ponto L.L.
        • Parvizi J.
        • Hichwa R.D.
        Subcortical and cortical brain activity during the feeling of self-generated emotions.
        Nat Neurosci. 2000; 3: 1049-1056
        • Damasio H.
        • Grabowski T.
        • Frank R.
        • Galaburda A.M.
        • Damasio A.R.
        The return of Phineas Gage: clues about the brain from the skull of a famous patient.
        Science. 1994; 264: 1102-1105
      1. Darwin C (1872/1965): The Expression of the Emotions in Man and Animals. Chicago: University of Chicago Press.

        • Davidson R.J.
        • Putnam K.M.
        • Larson C.L.
        Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence.
        Science. 2000; 289: 591-594
        • Donegan N.H.
        • Sanislow C.A.
        • Blumberg H.P.
        • Fulbright R.K.
        • Lacadie C.
        • Skudlarski P.
        • et al.
        Amygdala hyperreactivity in borderline personality disorder: implications for emotional dysregulation.
        Biol Psychiatry. 2003; 54: 1284-1293
        • Dougherty D.D.
        • Rauch S.L.
        • Deckersbach T.
        • Marci C.
        • Loh R.
        • Shin L.M.
        • et al.
        Ventromedial prefrontal cortex and amygdala dysfunction during an anger induction positron emission tomography study in patients with major depressive disorder with anger attacks.
        Arch Gen Psychiatry. 2004; 61: 795-804
        • Dougherty D.D.
        • Shin L.M.
        • Alpert N.M.
        • Pitman R.K.
        • Orr S.P.
        • Lasko M.
        • et al.
        Anger in healthy men: a PET study using script-driven imagery.
        Biol Psychiatry. 1999; 46: 466-472
        • Ekman P.
        Emotions revealed: recognizing faces and feelings to improve communication and emotional life. Henry Holt and Company, LLC, New York2003
        • Ekman P.
        • Friesen W.V.
        Pictures of Facial Affect. Consulting Psychologists Press, Palo Alto1976
        • First M.B.
        • Spitzer R.L.
        • Williams J.B.W.
        • Gibbon M.
        Structured Clinical Interview for DSMIV-Patient Edition (SCID-P). American Psychiatric Press, Washington, DC1995
        • Fitzgerald D.A.
        • Angstadt M.
        • Jelsone L.M.
        • Nathan P.J.
        • Phan K.L.
        Beyond threat: Amygdala reactivity across multiple expressions of facial affect.
        Neuroimage. 2006; 30: 1441-1448
        • Friston K.J.
        • Buechel C.
        • Fink G.R.
        • Morris J.
        • Rolls E.
        • Dolan R.J.
        Psychophysiological and modulatory interactions in neuroimaging.
        Neuroimage. 1997; 6: 218-229
        • Friston K.J.
        • Holmes A.P.
        • Worsley K.J.
        • Poline J.B.
        • Frith C.D.
        • Frackowiak R.S.
        Statistical parametric maps in functional imaging: A general linear approach.
        Hum Brain Mapp. 1995; : 189-210
        • Fu C.H.
        • Williams S.C.
        • Cleare A.J.
        • Brammer M.J.
        • Walsh N.D.
        • Kim J.
        • et al.
        Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study.
        Arch Gen Psychiatry. 2004; 61: 877-889
        • Genovese C.R.
        • Lazar N.A.
        • Nichols T.
        Thresholding of statistical maps in functional neuroimaging using the false discovery rate.
        Neuroimage. 2002; 15: 870-878
        • Ghashghaei H.T.
        • Barbas H.
        Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey.
        Neuroscience. 2002; 115: 1261-1279
        • Grafman J.
        • Schwab K.
        • Warden D.
        • Pridgen A.
        • Brown H.R.
        • Salazar A.M.
        Frontal lobe injuries, violence, and aggression: a report of the Vietnam Head Injury Study.
        Neurology. 1996; 46: 1231-1238
        • Gusnard D.A.
        • Raichle M.E.
        Searching for a baseline: functional imaging and the resting human brain.
        Nat Rev Neurosci. 2001; 2: 685-694
        • Harmer C.J.
        • Thilo K.V.
        • Rothwell J.C.
        • Goodwin G.M.
        Transcranial magnetic stimulation of medial-frontal cortex impairs the processing of angry facial expressions.
        Nat Neurosci. 2001; 4: 17-18
        • Herpertz S.C.
        • Dietrich T.M.
        • Wenning B.
        • Krings T.
        • Erberich S.G.
        • Willmes K.
        • et al.
        Evidence of abnormal amygdala functioning in borderline personality disorder: a functional MRI study.
        Biol Psychiatry. 2001; 50: 292-298
        • Izquierdo A.
        • Murray E.A.
        Combined unilateral lesions of the amygdala and orbital prefrontal cortex impair affective processing in rhesus monkeys.
        J Neurophysiol. 2004; 91: 2023-2039
        • Izquierdo A.
        • Suda R.K.
        • Murray E.A.
        Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency.
        J Neurosci. 2004; 24: 7540-7548
        • Izquierdo A.
        • Suda R.K.
        • Murray E.A.
        Comparison of the effects of bilateral orbitofrontal cortex lesions and amygdala lesions on emotional responses in rhesus monkeys.
        J Neurosci. 2005; 25: 8534-8542
        • Juengling F.D.
        • Schmahl C.
        • Hesslinger B.
        • Ebert D.
        • Bremner J.D.
        • Gostomzyk J.
        • et al.
        Positron emission tomography in female patients with borderline personality disorder.
        J Psychiatr Res. 2003; 37: 109-115
        • Kessler R.C.
        • Coccaro E.F.
        • Fava M.
        • Jaeger S.
        • Jin R.
        • Walters E.
        The prevalence and correlates of DSM-IV Intermittent Explosive Disorder in the National Comorbidity Survey Replication.
        Arch Gen Psychiatry. 2006; 63: 669-678
        • Kiehl K.A.
        • Smith A.M.
        • Hare R.D.
        • Mendrek A.
        • Forster B.B.
        • Brink J.
        • Liddle P.F.
        Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging.
        Biol Psychiatry. 2001; 50: 677-684
        • Klein D.N.
        • Ouimette P.C.
        • Kelly H.S.
        • Ferro T.
        • Riso L.P.
        Test-retest reliability of team consensus best-estimate diagnoses of axis I and II disorders in a family study.
        Am J Psychiatry. 1994; 151: 1043-1047
        • Kluver H.
        • Bucy P.C.
        Preliminary analysis of functions of the temporal lobes in monkeys.
        Arch Neurol Psychiatry. 1939; 42: 979-1000
        • Kosten T.A.
        • Rounsaville B.J.
        Sensitivity of psychiatric diagnosis based on the best estimate procedure.
        Am J Psychiatry. 1992; 149: 1225-1227
        • Kringelbach M.L.
        • Rolls E.T.
        The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology.
        Prog Neurobiol. 2004; 72: 341-372
        • Kumpfel T.
        • Lechner C.
        • Auer D.
        • Kraft E.
        • Lydtin H.
        • Trenkwalder C.
        Non-convulsive status epilepticus with marked neuropsychiatric manifestations and MRI changes after treatment of hypercalcaemia.
        Acta Neurol Scand. 2000; 102: 337-339
        • Leckman J.F.
        • Sholomskas D.
        • Thompson W.D.
        • Belanger A.
        • Weissman M.M.
        Best estimate of lifetime psychiatric diagnosis: a methodological study.
        Arch Gen Psychiatry. 1982; 39: 879-883
        • McCloskey M.S.
        • Berman M.E.
        • Noblett K.L.
        • Coccaro E.F.
        Intermittent explosive disorder-integrated research diagnostic criteria: convergent and discriminant validity.
        J Psychiatr Res. 2006; 40: 231-242
        • Muller J.L.
        • Sommer M.
        • Wagner V.
        • Lange K.
        • Taschler H.
        • Roder C.H.
        • 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.
        Biol Psychiatry. 2003; 54: 152-162
        • New A.S.
        • Buchsbaum M.S.
        • Hazlett E.A.
        • Goodman M.
        • Koenigsberg H.W.
        • Lo J.
        • et al.
        Fluoxetine increases relative metabolic rate in prefrontal cortex in impulsive aggression.
        Psychopharmacology (Berl). 2004; 176: 451-458
        • New A.S.
        • Hazlett E.A.
        • Buchsbaum M.S.
        • Goodman M.
        • Reynolds D.
        • Mitropoulou V.
        • et al.
        Blunted prefrontal cortical 18fluorodeoxyglucose positron emission tomography response to meta-chlorophenylpiperazine in impulsive aggression.
        Arch Gen Psychiatry. 2002; 59: 621-629
        • Noll D.C.
        • Stenger V.A.
        • Vazquez A.L.
        • Peltier S.J.
        Spiral scanning in functional MRI.
        in: Moonen C. Bandettini P.A. Medical Radiology: Functional MRI. Springer-Verlag, Heidelberg1999
        • Nomura M.
        • Ohira H.
        • Haneda K.
        • Iidaka T.
        • Sadato N.
        • Okada T.
        • Yonekura Y.
        Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study.
        Neuroimage. 2004; 21: 352-363
        • Ochsner K.N.
        • Gross J.J.
        The cognitive control of emotion.
        Trends Cogn Sci. 2005; 9: 242-249
        • Ongur D.
        • Ferry A.T.
        • Price J.L.
        Architectonic subdivision of the human orbital and medial prefrontal cortex.
        J Comp Neurol. 2003; 460: 425-449
        • Pfohl B.
        • Blum N.
        • Zimmerman M.
        Structured Clinical Interview for DSM-IV Personality. 1995
        • Phan K.L.
        • Wager T.
        • Taylor S.F.
        • Liberzon I.
        Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI.
        Neuroimage. 2002; 16: 331-348
        • Pribram K.
        • Bragshaw M.
        Further analysis of the temporal lobe syndrome utilizing frontotemporal ablation.
        J Comparative Neurology. 1953; 99: 347-375
        • Price J.L.
        Comparative aspects of amygdala connectivity.
        Ann N Y Acad Sci. 2003; 985: 50-58
        • Raine A.
        • Buchsbaum M.
        • LaCasse L.
        Brain abnormalities in murderers indicated by positron emission tomography.
        Biol Psychiatry. 1997; 42: 495-508
        • Raine A.
        • Buchsbaum M.S.
        • Stanley J.
        • Lottenberg S.
        • Abel L.
        • Stoddard J.
        Selective reductions in prefrontal glucose metabolism in murderers.
        Biol Psychiatry. 1994; 36: 365-373
        • Raine A.
        • Lencz T.
        • Bihrle S.
        • LaCasse L.
        • Colletti P.
        Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder.
        Arch Gen Psychiatry. 2000; 57 (discussion 128–129.): 119-127
        • Raine A.
        • Meloy J.R.
        • Bihrle S.
        • Stoddard J.
        • LaCasse L.
        • Buchsbaum M.S.
        Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers.
        Behav Sci Law. 1998; 16: 319-332
        • Saddoris M.P.
        • Gallagher M.
        • Schoenbaum G.
        Rapid associative encoding in basolateral amygdala depends on connections with orbitofrontal cortex.
        Neuron. 2005; 46: 321-331
        • Schmahl C.G.
        • Vermetten E.
        • Elzinga B.M.
        • Bremner J.D.
        A positron emission tomography study of memories of childhood abuse in borderline personality disorder.
        Biol Psychiatry. 2004; 55: 759-765
        • Schneider F.
        • Habel U.
        • Kessler C.
        • Posse S.
        • Grodd W.
        • Muller-Gartner H.W.
        Functional imaging of conditioned aversive emotional responses in antisocial personality disorder.
        Neuropsychobiology. 2000; 42: 192-201
        • Sheline Y.I.
        • Barch D.M.
        • Donnelly J.M.
        • Ollinger J.M.
        • Snyder A.Z.
        • Mintun M.A.
        Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study.
        Biol Psychiatry. 2001; 50: 651-658
        • Siever L.J.
        • Buchsbaum M.S.
        • New A.S.
        • Spiegel-Cohen J.
        • Wei T.
        • Hazlett E.A.
        • et al.
        d,l-fenfluramine response in impulsive personality disorder assessed with [18F]fluorodeoxyglucose positron emission tomography.
        Neuropsychopharmacology. 1999; 20: 413-423
        • Soloff P.H.
        • Meltzer C.C.
        • Becker C.
        • Greer P.J.
        • Kelly T.M.
        • Constantine D.
        Impulsivity and prefrontal hypometabolism in borderline personality disorder.
        Psychiatry Res. 2003; 123: 153-163
        • Soloff P.H.
        • Meltzer C.C.
        • Greer P.J.
        • Constantine D.
        • Kelly T.M.
        A fenfluramine-activated FDG-PET study of borderline personality disorder.
        Biol Psychiatry. 2000; 47: 540-547
        • Somerville L.H.
        • Kim H.
        • Johnstone T.
        • Alexander A.L.
        • Whalen P.J.
        Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety.
        Biol Psychiatry. 2004; 55: 897-903
        • Spielberger
        State-Trait Anger Expression Inventory: Professional manual. 1996
        • Sterzer P.
        • Stadler C.
        • Krebs A.
        • Kleinschmidt A.
        • Poustka F.
        Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder.
        Biol Psychiatry. 2005; 57: 7-15
        • Strauss M.M.
        • Makris N.
        • Aharon I.
        • Vangel M.G.
        • Goodman J.
        • Kennedy D.N.
        • et al.
        fMRI of sensitization to angry faces.
        Neuroimage. 2005; 26: 389-413
        • Tebartz van Elst L.
        • Hesslinger B.
        • Thiel T.
        • Geiger E.
        • Haegele K.
        • Lemieux L.
        • et al.
        Frontolimbic brain abnormalities in patients with borderline personality disorder: a volumetric magnetic resonance imaging study.
        Biol Psychiatry. 2003; 54: 163-171
        • Tzourio-Mazoyer N.
        • Landeau B.
        • Papathanassiou D.
        • Crivello F.
        • Etard O.
        • Delcroix N.
        • et al.
        Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.
        Neuroimage. 2002; 15: 273-289
        • Urry H.L.
        • van Reekum C.M.
        • Johnstone T.
        • Kalin N.H.
        • Thurow M.E.
        • Schaefer H.S.
        • et al.
        Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults.
        J Neurosci. 2006; 26: 4415-4425
        • van Elst L.T.
        • Woermann F.G.
        • Lemieux L.
        • Thompson P.J.
        • Trimble M.R.
        Affective aggression in patients with temporal lobe epilepsy: a quantitative MRI study of the amygdala.
        Brain. 2000; 123: 234-243
        • Walter B.
        • Blecker C.
        • Kirsch P.
        • et al.
        MARINA: An easy to use tool for the creation of MAsks for Interest Analyses.
        Neuroimage. 2003; 19: S47
        • Walz N.C.
        • Benson B.A.
        Labeling and discrimination of facial expressions by aggressive and nonaggressive men with mental retardation.
        Am J Ment Retard. 1996; 101: 282-291
        • Woermann F.G.
        • van Elst L.T.
        • Koepp M.J.
        • Free S.L.
        • Thompson P.J.
        • Trimble M.R.
        • Duncan J.S.
        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.
        J Neurol Neurosurg Psychiatry. 2000; 68: 162-169
        • Worsley K.J.
        • Marrett P.
        • Neelin A.C.
        • Friston K.J.
        • Evans A.C.
        A unified statistical approach for determining significant signals in images of cerebral activation.
        Hum Brain Mapp. 1996; 4: 58-73
        • Wright P.
        • Liu Y.
        Neutral faces activate the amygdala during identity matching.
        NeuroImage. 2005; 29: 628-636