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Original article| Volume 48, ISSUE 1, P43-50, July 01, 2000

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Activation of anterior paralimbic structures during guilt-related script-driven imagery

  • Lisa M Shin
    Correspondence
    Address reprint requests to Lisa M. Shin, Ph.D., Tufts University, Department of Psychology, 490 Boston Avenue, Medford MA 02155
    Affiliations
    Department of Psychology, Tufts University, Medford, Massachusetts, USA (LMS)

    Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (LMS, DDD, SPO, RKP, SLR)
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  • Darin D Dougherty
    Affiliations
    Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (LMS, DDD, SPO, RKP, SLR)

    Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (DDD, NMA, AJF, SLR)
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  • Scott P Orr
    Affiliations
    Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (LMS, DDD, SPO, RKP, SLR)

    VA Research Service, Manchester, New Hampshire, USA (SPO, RKP, ML, MLM)
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  • Roger K Pitman
    Affiliations
    Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (LMS, DDD, SPO, RKP, SLR)

    VA Research Service, Manchester, New Hampshire, USA (SPO, RKP, ML, MLM)
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  • Mark Lasko
    Affiliations
    VA Research Service, Manchester, New Hampshire, USA (SPO, RKP, ML, MLM)
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  • Michael L Macklin
    Affiliations
    VA Research Service, Manchester, New Hampshire, USA (SPO, RKP, ML, MLM)
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  • Nathaniel M Alpert
    Affiliations
    Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (DDD, NMA, AJF, SLR)
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  • Alan J Fischman
    Affiliations
    Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (DDD, NMA, AJF, SLR)
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  • Scott L Rauch
    Affiliations
    Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (LMS, DDD, SPO, RKP, SLR)

    Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, MassachusettsUSA (DDD, NMA, AJF, SLR)
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      Abstract

      Background: Several recent neuroimaging studies have examined the neuroanatomical correlates of normal emotional states, such as happiness, sadness, fear, anger, anxiety, and disgust; however, no previous study has examined the emotional state of guilt.
      Methods: In the current study, we used positron emission tomography and the script-driven imagery paradigm to study regional cerebral blood flow (rCBF) during the transient emotional experience of guilt in eight healthy male participants. In the Guilt condition, participants recalled and imagined participating in a personal event involving the most guilt they had ever experienced. In the Neutral condition, participants recalled and imagined participating in an emotionally neutral personal event.
      Results: In the Guilt versus Neutral comparison, rCBF increases occurred in anterior paralimbic regions of the brain: bilateral anterior temporal poles, anterior cingulate gyrus, and left anterior insular cortex/inferior frontal gyrus.
      Conclusions: These results, along with those of previous studies, are consistent with the notion that anterior paralimbic regions of the brain mediate negative emotional states in healthy individuals.

      Keywords

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      References

        • Aggleton J.P.
        • Burton M.J.
        • Passingham R.E.
        Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta).
        Brain Res. 1980; 190: 347-368
        • Anand B.K.
        • Dua S.
        Circulating and respiratory changes induced by electrical stimulation of limbic system (visceral brain).
        J Neurophysiol. 1956; 19: 393-400
        • Benkelfat C.
        • Bradwejn J.
        • Meyer E.
        • Ellenbogen M.
        • Milot S.
        • Gjedde A.
        • et al.
        Functional neuroanatomy of CCK4-induced anxiety in normal healthy volunteers.
        Am J Psychiatry. 1995; 152: 1180-1184
        • Berrios G.E.
        • Bulbena A.
        • Bakshi N.
        • Dening T.R.
        • Jenaway A.
        • Markar H.
        • et al.
        Feelings of guilt in major depression.
        Br J Psychiatry. 1992; 160: 781-787
        • Bush G.
        • Whalen P.J.
        • Rosen B.R.
        • Jenike M.A.
        • McInerney S.C.
        • Rauch S.L.
        The Counting Stroop.
        Hum Brain Map. 1998; 6: 270-282
        • Chua P.
        • Krams M.
        • Toni I.
        • Passingham R.
        • Dolan R.
        A functional anatomy of anticipatory anxiety.
        Neuroimage. 1999; 9: 563-571
        • Coghill R.C.
        • Talbot J.D.
        • Evans A.C.
        • Meyer E.
        • Gjedde A.
        • Bushnell M.C.
        • et al.
        Distributed processing of pain and vibration by the human brain.
        J Neurosci. 1994; 14: 4095-4108
        • Cottraux J.
        • Gérard D.
        • Cinotti L.
        • Froment J.-C.
        • Deiber M.-P.
        • Le Bars D.
        • et al.
        A controlled positron emission tomography study of obsessive and neutral auditory stimulation in obsessive-compulsive disorder with checking rituals.
        Psychiatry Res. 1996; 60: 101-112
        • Devinsky O.
        • Morrell M.J.
        • Vogt B.A.
        Contributions of anterior cingulate cortex to behaviour.
        Brain. 1995; 118: 279-306
        • Dougherty D.D.
        • Shin L.M.
        • Alpert N.M.
        • Pitman R.K.
        • Orr S.P.
        • Lasko M.
        • et al.
        Anger in healthy men.
        Biol Psychiatry. 1999; 46: 466-472
        • Drevets W.C.
        • Videen T.O.
        • MacLeod A.K.
        • Haller J.W.
        • Raichle M.E.
        PET images of blood flow changes during anxiety.
        Science. 1992; 256: 1696
        • Fischer H.
        • Wik G.
        • Fredrikson M.
        Functional neuroanatomy of robbery re-experience.
        Neuroreport. 1996; 7: 2081-2086
        • Francis S.
        • Rolls E.T.
        • Bowtell R.
        • McGlone F.
        • O’Doherty J.
        • Browning A.
        • et al.
        The representation of pleasant touch in the brain and its relationship with taste and olfactory areas.
        Neuroreport. 1999; 10: 453-459
      1. Frijda NH (1994): Universal antecedents exist, and are interesting. In: Ekman P, Davidson RJ, editors. The Nature of Emotion: Fundamental Questions. New York: Oxford University Press, 155–162.

        • Friston K.J.
        • Frith C.D.
        • Liddle P.F.
        • Frakowiak R.S.J.
        Comparing functional (PET) images.
        J Cereb Blood Flow Metab. 1991; 11: 690-699
        • Friston K.J.
        • Holmes A.P.
        • Worsley K.J.
        • Poline J.-P.
        • Frith C.D.
        • Frackowiak R.S.J.
        Statistical parametric maps in functional imaging.
        Hum Brain Map. 1995; 2: 189-210
        • George M.S.
        • Ketter T.A.
        • Parekh P.I.
        • Herscovitch P.
        • Post R.M.
        Gender differences in regional cerebral blood flow during transient self-induced sadness or happiness.
        Biol Psychiatry. 1996; 40: 859-871
        • George M.S.
        • Ketter T.A.
        • Parekh P.I.
        • Horowitz B.
        • Herscovitch P.
        • Post R.M.
        Brain activity during transient sadness and happiness in healthy women.
        Am J Psychiatry. 1995; 152: 341-351
        • Henning K.R.
        • Frueh B.C.
        Combat guilt and its relationship to PTSD symptoms.
        J Clin Psychol. 1997; 53: 801-808
        • Kaada B.R.
        • Pribram K.H.
        • Epstein J.A.
        Respiratory and vascular responses in monkeys from temporal pole, insula, orbital surface and cingulate gyrus.
        J Neurophysiol. 1949; 12: 347-356
        • Ketter T.A.
        • Andreason P.J.
        • George M.S.
        • Lee C.
        • Gill D.S.
        • Parekh P.I.
        • et al.
        Anterior paralimbic mediation of procaine-induced emotional and psychosensory experiences.
        Arch Gen Psychiatry. 1996; 53: 59-69
        • Kimbrell T.A.
        • George M.S.
        • Parekh P.I.
        • Ketter T.A.
        • Podell D.M.
        • Danielson A.L.
        • et al.
        Regional brain activity during transient self-induced anxiety and anger in healthy adults.
        Biol Psychiatry. 1999; 46: 454-465
        • Kosslyn S.M.
        • Shin L.M.
        • Thompson W.L.
        • McNally R.J.
        • Rauch S.L.
        • Pitman R.K.
        • et al.
        Neural effects of visualizing and perceiving aversive stimuli.
        Neuroreport. 1996; 7: 1569-1576
        • LaBar K.S.
        • Gatenby C.
        • Gore J.C.
        • LeDoux J.E.
        • Phelps E.A.
        Human amygdala activation during conditioned fear acquisition and extinction.
        Neuron. 1998; 20: 937-945
        • Lane R.D.
        • Fink G.R.
        • Chau P.M.-L.
        • Dolan R.J.
        Neural activation during selective attention to subjective emotional responses.
        Neuroreport. 1997; 8: 3969-3972
        • Lane R.D.
        • Reiman E.M.
        • Ahern G.L.
        • Schwartz G.E.
        • Davidson R.J.
        Neuroanatomical correlates of happiness, sadness, and disgust.
        Am J Psychiatry. 1997; 154: 926-933
        • Lang P.J.
        The cognitive psychophysiology of emotion.
        in: Tuma A.H. Maser J. Anxiety and the Anxiety Disorders. Lawrence Erlbaum, Hillsdale, NJ1985
        • Lang P.J.
        • Levin D.N.
        • Miller G.A.
        • Kozak M.J.
        Fear behavior, fear imagery, and the psychophysiology of emotion.
        J Abnorm Psychol. 1983; 92: 276-306
        • LeDoux J.E.
        Emotion and the amygdala.
        in: Aggleton J.P. The Amygdala Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York1992
      2. Levenson RW (1994): The search for autonomic specificity. In: Ekman P, Davidson RJ, editors. The Nature of Emotion: Fundamental Questions. New York: Oxford University Press, 252–257.

        • Mayberg H.S.
        • Brannan S.K.
        • Mahurin R.K.
        • Jerabek P.A.
        • Brickman J.S.
        • Tekell J.L.
        • et al.
        Cingulate function in depression.
        Neuroreport. 1997; 8: 1057-1061
        • Mesulam M.-M.
        Principles of Behavioral Neurology. F.A. Davis, Philadelphia1985
        • Mesulam M.-M.
        • Mufson E.J.
        Insula of the old world monkey. I.
        J Comp Neurol. 1982; 212: 1-22
        • Mesulam M.-M.
        • Mufson E.J.
        Insula of the old world monkey. III.
        J Comp Neurol. 1982; 212: 38-52
        • Mufson E.J.
        • Mesulam M.-M.
        Insula of the old world monkey. II.
        J Comp Neurol. 1982; 212: 23-37
        • Morris J.S.
        • Frith C.D.
        • Perrett D.I.
        • Rowland D.
        • Young A.W.
        • Calder A.J.
        • et al.
        A differential response in the human amygdala to fearful and happy facial expressions.
        Nature. 1996; 383: 812-815
        • Mullan S.
        • Penfield W.
        Illusions of comparative interpretation and emotion.
        Arch Neurol Psychiatry. 1959; 81: 269-284
        • Oldfield R.C.
        The assessment and analysis of handedness.
        Neuropsychologia. 1971; 9: 97-113
        • Orr S.P.
        • Lasko N.B.
        • Metzger L.J.
        • Berry N.J.
        • Ahern C.E.
        • Pitman R.K.
        Psychophysiologic assessment of women with posttraumatic stress disorder resulting from childhood sexual abuse.
        J Consult Clin Psychol. 1998; 66: 906-913
        • Paradiso S.
        • Robinson R.G.
        • Andreasen N.C.
        • Downhill J.E.
        • Davidson R.J.
        • Kirchner P.T.
        • et al.
        Emotional activation of limbic circuitry in elderly normal subjects in a PET study.
        Am J Psychiatry. 1997; 154: 384-389
        • Pardo J.V.
        • Pardo P.J.
        • Janer K.W.
        • Raichle M.E.
        The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm.
        Proc Natl Acad Sci U S A. 1990; 87: 256-259
        • Pardo J.V.
        • Pardo P.J.
        • Raichle M.E.
        Neural correlates of self-induced dysphoria.
        Am J Psychiatry. 1993; 150: 713-719
        • Phillips M.L.
        • Young A.W.
        • Senior C.
        • Brammer M.
        • Andrew C.
        • Calder A.J.
        • et al.
        A specific neural substrate for perceiving facial expressions of disgust.
        Nature. 1997; 389: 495-498
        • Pitman R.K.
        • Orr S.P.
        • Forgue D.F.
        • Altman B.
        • de Jong J.B.
        • Herz L.R.
        Psychophysiologic responses to combat imagery of Vietnam veterans with post-traumatic stress disorder vs. other anxiety disorders.
        J Abnorm Psychol. 1990; 99: 49-54
        • Pitman R.K.
        • Orr S.P.
        • Forgue D.F.
        • de Jong J.B.
        • Claiborn J.M.
        Psychophysiologic assessment of posttraumatic stress disorder imagery in Vietnam combat veterans.
        Arch Gen Psychiatry. 1987; 44: 970-975
        • Rauch S.L.
        • Jenike M.A.
        • Alpert N.M.
        • Baer L.
        • Breiter H.C.R.
        • Savage C.R.
        • et al.
        Regional cerebral blood flow measured during symptom provocation in obsessive-compulsive disorder using oxygen 15-labeled carbon dioxide and positron emission tomography.
        Arch Gen Psychiatry. 1994; 51: 62-70
        • Rauch S.L.
        • Savage C.R.
        • Alpert N.M.
        • Miguel E.C.
        • Baer L.
        • Breiter H.C.
        • et al.
        A positron emission tomographic study of simple phobic symptom provocation.
        Arch Gen Psychiatry. 1995; 52: 20-28
        • Rauch S.L.
        • Shin L.M.
        • Dougherty D.
        • Alpert N.M.
        • Orr S.P.
        • Lasko M.
        • et al.
        Neural activation during sexual and competitive arousal in healthy men.
        Psychiatry Res Neuroimag. 1999; 91: 1-10
        • Rauch S.L.
        • van der Kolk B.A.
        • Fisler R.E.
        • Alpert N.M.
        • Orr S.P.
        • Savage C.R.
        • et al.
        A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery.
        Arch Gen Psychiatry. 1996; 53: 380-387
        • Reiman E.M.
        • Lane R.D.
        • Ahern G.L.
        • Schwartz G.E.
        • Davidson R.J.
        • Friston K.J.
        • et al.
        Neuroanatomical correlates of externally and internally generated human emotion.
        Am J Psychiatry. 1997; 154: 918-925
        • Schneider F.
        • Grodd W.
        • Weiss U.
        • Klose U.
        • Mayer K.R.
        • Nägele T.
        • et al.
        Functional MRI reveals left amygdala activation during emotion.
        Psychiatry Res Neuroimag. 1997; 76: 75-82
        • Schneider F.
        • Gur R.E.
        • Mozley L.H.
        • Smith R.J.
        • Mozley P.D.
        • Censits D.M.
        • et al.
        Mood effects on limbic blood flow correlate with emotional self-rating.
        Psychiatry Res Neuroimag. 1995; 61: 265-283
        • Schneider R.J.
        • Friedman D.P.
        • Mishkin M.
        A modality-specific somatosensory area within the insula of the rhesus monkey.
        Brain Res. 1993; 621: 116-120
        • Servan-Schreiber D.
        • Perlstein W.M.
        • Cohen J.D.
        • Mintun M.
        Selective pharmacological activation of limbic structures in human volunteers.
        J Neuropsychiatry Clin Neurosci. 1998; 10: 148-159
        • Shin L.M.
        • Kosslyn S.M.
        • McNally R.J.
        • Alpert N.M.
        • Thompson W.L.
        • Rauch S.L.
        • et al.
        Visual imagery and perception in posttraumatic stress disorder.
        Arch Gen Psychiatry. 1997; 54: 233-241
        • Shin L.M.
        • McNally R.J.
        • Kosslyn S.M.
        • Thompson W.L.
        • Rauch S.L.
        • Alpert N.M.
        • et al.
        Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related posttraumatic stress disorder.
        Am J Psychiatry. 1999; 156: 575-584
        • Small D.M.
        • Zald D.H.
        • Jones-Gotman M.
        • Zatorre R.J.
        • Pardo J.V.
        • Frey S.
        • et al.
        Human cortical gustatory areas.
        Neuroreport. 1999; 10: 7-14
        • Spitzer R.L.
        • Williams J.B.W.
        • Gibbon M.
        • First M.
        Structured Clinical Interview for DSM-III-R (SCID). American Psychiatric Press, Washington, DC1990
        • Talairach J.
        • Tournoux P.
        Co-Planar Stereotaxic Atlas of the Human Brain. Thieme, Stuttgart, Germany1988
        • Vogt B.A.
        • Finch D.M.
        • Olson C.R.
        Functional heterogeneity in cingulate cortex.
        Cereb Cortex. 1992; 2: 435-443
        • Vogt B.A.
        • Nimchinsky E.A.
        • Vogt L.J.
        • Hof P.R.
        Human cingulate cortex.
        J Comp Neurol. 1995; 359: 490-506
        • Whalen P.J.
        Fear, vigilance, and ambiguity.
        Curr Dir Psychol Sci. 1998; 7: 177-188
        • Whalen P.J.
        • Bush G.
        • McNally R.J.
        • Wilhelm S.
        • McInerney S.C.
        • Jenike M.A.
        • et al.
        The Emotional Counting Stroop paradigm.
        Biol Psychiatry. 1998; 44: 1219-1228
        • Whalen P.J.
        • Rauch S.L.
        • Etcoff N.L.
        • McInerney S.C.
        • Lee M.B.
        • Jenike M.A.
        Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge.
        J Neurosci. 1998; 18: 411-418
        • Zald D.H.
        • Lee J.T.
        • Fluegel K.W.
        • Pardo J.V.
        Aversive gustatory stimulation activates limbic circuits in humans.
        Brain. 1998; 121: 1143-1154