Journal of Traumatic Stress

, Volume 8, Issue 4, pp 527–553 | Cite as

Functional neuroanatomical correlates of the effects of stress on memory

  • J. Douglas Bremner
  • John H. Krystal
  • Steven M. Southwick
  • Dennis S. Charney


Recently there has been an increase in interest in the relationship between stress and memory. Brain regions which are involved in memory function also effect the stress response. Traumatic stress results in changes in these brain regions; alterations in these brain regions in turn may mediate symptoms of posttraumatic stress disorder (PTSD). Neural mechanisms which are relevant to the effects of stress on memory, such as fear conditioning, stress sensitization, and extinction, are reviewed in relation to their implications for PTSD. Special topics including neural mechanisms in dissociation, neurobiological approaches to the validity of childhood memories as they apply to controversies over the “False Memory Syndrome,” and implications of the effects of stress on memory for psychotherapy, are also reviewed. The findings discussed in this paper are consistent with the formulation that stress-induced alterations in brain regions and systems involved in memory may underlie many of the symptoms of PTSD, as well as dissociative amnesia, seen in survivors of traumatic stress.

Key words

PTSD dissociation memory amygdala hippocampus amnesia trauma stress neurobiology 


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  1. Armanini, M. P., Hutchins, C., Stein, B. A., & Sapolsky, R. M. (1990). Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent.Brain Research, 532 7–1.CrossRefPubMedGoogle Scholar
  2. Borrell, J., De Kloet, E. R., Versteeg, D. H. G., & Bohus, B. (1983). Inhibitory avoidance deficit following short-term adrenalectomy in the rat: The role of adrenal catecholamines.Behavioral Neurology and Biology, 39 241.CrossRefGoogle Scholar
  3. Bower, G. H. (1981). Mood and memory.American Psychologist, 36 129–148.CrossRefPubMedGoogle Scholar
  4. Bremner, J. D., Davis, M., Southwick, S. M., Krystal, J. H., & Charney, D. S. (1993). The neurobiology of posttraumatic stress disorder. In J. M. Oldham, M. G. Riba, & A. Tasman (Eds.),Review of Psychiatry, Vol. 12 (pp. 182–204). Washington, DC: American Psychiatric Press.Google Scholar
  5. Bremner, J. D., Ng, C. K., Staib, L., Markey, J., Duncan, J., Zubal, G., Krystal, J. H., Mazza, S., Rich, D., Southwick, S. M., Capelli, S., Seibyl, J. P., Dey, H., Soufer, R., Charney, D. S., & Innis, R. B. (1992). PET measurement of cerebral metabolism following a noradrenergic challenge in patients with posttraumatic stress disorder and in healthy subjects (abst.).Journal of Nuclear Medicine, 34 205P-206P.Google Scholar
  6. Bremner, J. D., Randall, P., Scott, T. M., Bronen, R. A., Seibyl, J. P., Southwick, S. M., Delaney, R. C., McCarthy, G., Charney, D. S., & Innis, R. B. (1995). MRI-based measurement of hippocampal volume in combat-related posttraumatic stress disorder.American Journal of Psychiatry, 152 973–981.PubMedGoogle Scholar
  7. Bremner, J. D., Scott, T. M., Delaney, R. C., Southwick, S. M., Mason, J. W., Johnson, D. R., Innis, R. B., McCarthy, G., & Charney, D. S. (1993). Deficits in short-term memory in post-traumatic stress disorder.American Journal of Psychiatry, 150 1015–1019.PubMedGoogle Scholar
  8. Bremner, J. D., Southwick, S. M., Brett, E., Fontana, A., Rosenheck, R., & Charney, D. S. (1992). Dissociation and posttraumatic stress disorder in Vietnam combat veterans.American Journal of Psychiatry, 149 328–332.PubMedGoogle Scholar
  9. Bremner, J. D., Southwick, S. M., & Charney, D. S. (1994). Etiologic factors in the development of posttraumatic stress disorder. In C. M. Mazure (Ed.),Stress and psychiatric disorders (pp. 149–186). Washington, DC: American Psychiatric Press.Google Scholar
  10. Bremner, J. D., Southwick, S. M., Johnson, D. R., Yehuda, R., & Charney, D. S. (1993). Childhood physical abuse in combat-related posttraumatic stress disorder.American Journal of Psychiatry, 150 235–239.PubMedGoogle Scholar
  11. Bremner, J. D., Steinberg, M., Southwick, S. M., Johnson, D. R., & Charney, D. S. (1993). Use of the Structured Clinical Interview for DSMIV-Dissociative Disorders for systematic assessment of dissociative symptoms in posttraumatic stress disorder.American Journal of Psychiatry, 150 1011–1014.PubMedGoogle Scholar
  12. Butler, R. W., Braff, D. L., Rausch, J. L., Jenkins, M. A., Sprock, J., & Geyer, M. A. (1990). Physiological evidence of exaggerated startle response in a subgroup of Vietnam veterans with combat-related PTSD.American Journal of Psychiatry, 147 1308–1312.PubMedGoogle Scholar
  13. Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994). Alpha-adrenergic activation and memory for emotional events.Nature, 371 702–703.CrossRefPubMedGoogle Scholar
  14. Carlson, E. B., & Rosser-Hogan, R. (1991). Trauma experiences, posttraumatic stress, dissociation, and depression in Cambodian refugees.American Journal of Psychiatry, 148 1548–1552.PubMedGoogle Scholar
  15. Cassiday, K. L., McNally, R. J., & Zeitlin, S. B. (1992). Cognitive processing of trauma cues in rape victims with posttraumatic stress disorder.Cognitive Therapy Research, 16 283–295.CrossRefGoogle Scholar
  16. Ceci, S. J., & Bruck, M. (1993). Suggestibility of the child witness: A historical review and synthesis.Psychological Bulletin, 113 403–439.CrossRefPubMedGoogle Scholar
  17. Chapman, W. P., Schroeder, H. R., Guyer, G., Brazier, M. A. B., Fager, C., Poppen, J. L., Solomon, H. C., & Yakolev, P. I. (1954). Physiological evidence concerning the importance of the amygdaloid nuclear region in the integration of circulating functions and emotion in man.Science, 129 949–950.Google Scholar
  18. Charney, D. S., Deutch, A. Y., Krystal, J. H., Southwick, S. M., & Davis, M. (1993). Psychobiologic mechanisms of posttraumatic stress disorder.Archives of General Psychiatry, 50 294–299.Google Scholar
  19. Damasio, A. R. (1990). Category-related recognition defects as a clue to the neural substrates of knowledge.Trends in Neurosciences, 13 95–98.CrossRefPubMedGoogle Scholar
  20. Davis, M. (1992). The role of the amygdala in fear and anxiety.Annual Reviews of Neuroscience, 15 353–375.CrossRefGoogle Scholar
  21. De Wied, D., & Croiset, G. (1991). Stress modulation of learning and memory processes.Methods and Achievements in Experimental Pathology, 15 167–199.PubMedGoogle Scholar
  22. Foa, E. B., Feske, U., Murdock, T. B., Kozak, M. J., & McCarthy, P. R. (1991). Processing of threat-related information in rape victims.Journal of Abnormal Psychology, 100 156–162.CrossRefPubMedGoogle Scholar
  23. Gloor, P., Olivier, A., Quesney, L. F., Andermann, R., & Horowitz, S. (1982). The role of the limbic system in experiential phenomena of temporal lobe epilepsy.Annals of Neurology, 12 129–144.CrossRefPubMedGoogle Scholar
  24. Goldman, P. S. (1971). Functional development of the prefrontal cortex in early life and the problem of neuronal plasticity.Experimental Neurology, 32 366–387.CrossRefPubMedGoogle Scholar
  25. Goldman-Rakic, P. S. (1988). Topography of cognition: Parallel distributed networks in primate association cortex.Annual Reviews of Neuroscience, 11 137–156.CrossRefGoogle Scholar
  26. Gold, P. E., & van Buskirk, R. (1975). Facilitation of time-dependent memory processes with posttrial epinephrine injections.Behavioral Biology, 13 145–153.CrossRefPubMedGoogle Scholar
  27. Gold, P. E. (1992). A proposed neurobiological basis for regulating memory storage for significant events. In E. Winograd & U. Neisser (Eds.),Affect and accuracy in recall: Studies in “flashbulb memories” (pp. 141–161). London: Cambridge Press.Google Scholar
  28. Gunne, L. M., & Reis, D. J. (1963). Changes in brain catecholamines associated with electrical stimulation of amygdaloid nucleus.Life Science, 11 804–809.CrossRefGoogle Scholar
  29. Halgren, E., Walter, R. D., Cherlow, D. G., & Crandall, P. H. (1978). Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala.Brain, 101 83–117.PubMedGoogle Scholar
  30. Helweg-Larsen, P., Hoffmeyer, H., Kieler, J., Thaysen, E. H., Thaysen, J. H., Thygesen, P., & Wulff, M. H. (1952). Famine disease in German concentration camps: Complications and sequels.Acta Medica Scandinavica, 274 235–460.Google Scholar
  31. Hitchcock, J. M., & Davis, M. (1986). Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm.Behavioral Neuroscience, 100 11–22.CrossRefPubMedGoogle Scholar
  32. Hitchcock, J. M., & Davis, M. (1991). Efferent pathway of the amygdala involved in conditioned fear as measured with the fear-potentiated startle paradigm.Behavioral Neuroscience, 105 826–842.CrossRefPubMedGoogle Scholar
  33. Jarrell, T. W., Gentile, C. G., Romanski, L. M., McCabe, P. M., & Schneiderman, N. (1987). Involvement of cortical and thalamic auditory regions in retention of differential bradycardiac conditioning to acoustic conditioned stimuli in rabbits.Brain Research, 412 285–294.CrossRefPubMedGoogle Scholar
  34. Jonides, J., Smith, E. E., Koeppe, R. A., Awh, E., Minoshima, S., & Mintun, M. A. (1993). Spatial working memory in humans as revealed by PET.Nature, 363 623–625.CrossRefPubMedGoogle Scholar
  35. Keane, T. M., Fairbank, J. A., Caddell, J. M., & Zimering, R. T. (1989). Implosive (flooding) therapy reduces symptoms of PTSD in Vietnam combat veterans.Behavior Therapist, 20 245–260.Google Scholar
  36. Kihlstrom, J. F. (1987). The cognitive unconscious.Science, 237 1445–1452.PubMedGoogle Scholar
  37. Kihlstrom, J. F., Glisky, M. L., & Angiulo, M. J. (1994). Dissociative tendencies and dissociative disorders.Journal of Abnormal Psychology, 103 117–124.CrossRefPubMedGoogle Scholar
  38. Kim, J. J., & Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear.Science, 256 675–677.PubMedGoogle Scholar
  39. Koopman, C., Classen, C., & Spiegel, D. (1994). Predictors of posttraumatic stress symptoms among survivors of the Oakland/Berkeley, Calif., firestorm.American Journal of Psychiatry, 151 888–894.PubMedGoogle Scholar
  40. Krystal, J. H., Karper, L. P., Seibyl, J. P., Freeman, G. K., Delaney, R., Bremner, J. D., Heninger, G. R., Bowers, M. B., Jr., & Charney, D. S. (1994). Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans.Archives of General Psychiatry, 51 199–214.PubMedGoogle Scholar
  41. Krystal, J. H., Bennnett, A., Bremner, J. D., Southwick, S. M., & Charney, D. S. (in press). Toward a cognitive neuroscience of dissociation and altered memory functions in posttraumatic stress disorder. In M. J. Friedman, D. S. Charney, & A. Y. Deutch (Eds.),Neurobiological and clinical consequences of stress: From normal adaptation to PTSD, Washington DC: American Psychiatric Press.Google Scholar
  42. LeDoux, J. E. (1977). Emotion. InHandbook of physiology-The nervous system V (pp. 419–459).Google Scholar
  43. LeDoux, J. L. (1993). Emotional memory: In search of systems and synapses.Annals of the New York Academy of Sciences, 149–157.Google Scholar
  44. Liang, K. C., Juler, R. G., & McGaugh, J. L. (1986). Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system.Brain Research, 368 125–133.CrossRefPubMedGoogle Scholar
  45. Loftus, E. F., & Loftus, G. R. (1980). On the permanence of stored information in the human brain.American Psychologist, 35 409–420.CrossRefPubMedGoogle Scholar
  46. Loftus, E. F., Garry, M., & Feldman, J. (1994). Forgetting sexual trauma: What does it mean when 38% forget?Journal of Consulting and Clinical Psychology, 62 1177–1181.CrossRefPubMedGoogle Scholar
  47. Loftus, E. F., Polonsky, S., & Fullilove, M. T. (1994). Memories of childhood sexual abuse: Remembering and repressing.Psychology of Women Quarterly, 18 67–84.Google Scholar
  48. Loewenstein, R. J., & Putnam, F. (1988). A comparison study of dissociative symptoms in patients with partial-complex seizures, MPD, and PTSD.Dissociation, 1 17–23.Google Scholar
  49. Luine, V., Villages, M., Martinex, C., & McEwen, B. S. (1994). Repeated stress causes reversible impairments of spatial memory performance.Brain Research, 639 167–170.CrossRefPubMedGoogle Scholar
  50. Marmar, C. R., Weiss, D. S., Schlenger, W. E., Fairbank, J. A., Jordan, B. K., Kulka, R. A., & Hough, R. L. (1994). Peritraumatic dissociation and posttraumatic stress in male Vietnam theater veterans.American Journal of Psychiatry, 151 902–908.PubMedGoogle Scholar
  51. McEwen B. S., Gould, E. A., & Sakai, R. R. (1992). The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress.British Journal of Psychiatry, 160 18–24.Google Scholar
  52. McGaugh, J. L. (1989). Involvement of hormonal and neuromodulatory systems in the regulation of memory storage: Endogenous modulation of memory storage.Annual Review of Neurosciences, 12 255–287.CrossRefGoogle Scholar
  53. McGaugh, J. L. (1990). Significance and remembrance: The role of neuromodulatory systems.Psychological Sciences, 1 15–25.Google Scholar
  54. McNally, R. J., Kaspi, S. P., Riemann, B. C., & Zeitlin, S. B. (1990). Selective processing of threat cues in posttraumatic stress disorder.Journal of Abnormal Psychology, 99 398–402.CrossRefPubMedGoogle Scholar
  55. McNally, R. J., English, G. E., & Lipke, H. J. (1993). Assessment of intrusive cognition in PTSD: Use of the modified Streep canadigm.Journal of Traumatic Stress, 6 33–41.Google Scholar
  56. Mishkin, M. (1978). Memory in monkeys severely impaired by combined but not separate removal of amygdala and hippocampus.Nature, 173 297–298.CrossRefGoogle Scholar
  57. Morgan, M. A., & LeDoux, J. E. (1994). Medial orbital lesions increase resistance to extinction but do not affect acquisition of fear conditioning.Proceedings of the Society for Neuroscience, 2 1006.Google Scholar
  58. Moscovitch, M. (1985). Memory from infancy to old age: Implications for theories for normal and pathological memory.Annals of the New York Academy of Sciences, 444 78–96.PubMedGoogle Scholar
  59. Murray, E. A., & Mishkin, M. (1986). Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy.Journal of Neurosciences, 6 1991–2003.Google Scholar
  60. Nemiah, J. C. (1989). Janet redivivus: The centenary ofl'Automatisme Psychologique.American Journal of Psychiatry, 146 1527–1530.PubMedGoogle Scholar
  61. Pardo, J. V., Fox, P. T., & Raichle, M. E. (1991). Localization of a human system for sustained attention by positron emission tomography.Nature, 349 61–64.CrossRefPubMedGoogle Scholar
  62. Petersen, S. E., Fox, P. T., Posner, M. I., Mintun, M., & Raichle, M. E. (1988). Positron emission tomographic studies of the cortical anatomy of single-word processing.Nature, 331 585–589.CrossRefPubMedGoogle Scholar
  63. Phillips, R. G., & LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.Behavioral Neuroscience, 106 274–285.CrossRefPubMedGoogle Scholar
  64. Pitman, R. K. (1989). Posttraumatic stress disorder, hormones, and memory (editorial).Biological Psychiatry, 26 221–223.CrossRefPubMedGoogle Scholar
  65. Pitman, R. K., Orr, S. P., & Lasko, N. B. (1993). Effects of intranasal vasopressin and oxytocin on physiologic responding during personal combat imagery in Vietnam veterans with posttraumatic stress disorder.Psychiatry Research, 48 107–117.CrossRefPubMedGoogle Scholar
  66. Posner, M. I., Petersen, S. E., Fox, P. T., & Raichle, M. E. (1988). Localization of cognitive operations in the human brain.Science, 240 1627–1631.PubMedGoogle Scholar
  67. Prins, A., Kaloupek, D. G., & Keane, T. M. (in press). Psychophysiological evidence for autonomic arousal and startle in traumatized adult populations. In M. J. Friedman, D. S. Charney, & A. Y. Deutch (Eds.),Neurobiological and clinical consequences of stress: From normal adaptation to PTSD.Google Scholar
  68. Putnam, F. W., Guroff, J. J., Silberman, E. K., Barban, L., & Post, R. M. (1986). The clinical phenomenology of multiple personality disorder: Review of 100 recent cases.Journal of Clinical Psychiatry, 47 285–293.PubMedGoogle Scholar
  69. Rosen, J. B., & Davis, M. (1988). Enhancement of acoustic startle by electrical stimulation of the amygdala.Behavioral Neuroscience, 102 195–202.CrossRefPubMedGoogle Scholar
  70. Rosen, J. B., Hitchcock, J. M., Sananes, C. B., Miserendino, M. J., & Davis, M. (1991). A direct projection from the central nucleus of the amygdala to the acoustic startle pathway: Anterograde and retrograde tracing studies.Behavioral Neuroscience, 105 817–825.PubMedGoogle Scholar
  71. Sapolsky, R. M. (1985). A mechanism for glucocorticoid toxicity in the hippocampus: Increased neuronal vulnerability to metabolic insults.Journal of Neuroscience, 5 1228–1232.PubMedGoogle Scholar
  72. Sapolsky, R. M., Uno, H., Rebert, C. S., & Finch, C. E. (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates.Journal of Neuroscience, 10 2897–2902.PubMedGoogle Scholar
  73. Sarter, M., & Markowitsch, H. J. (1985). Involvement of the amygdala in learning and memory: A critical review, with emphasis on anatomical relationship.Behavioral Neuroscience, 99 342–380.CrossRefPubMedGoogle Scholar
  74. Save, E., Poucet, B., Foreman, N., & Buhot, M-C. (1992). Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation.Behavioral Neuroscience, 106 447–456.CrossRefPubMedGoogle Scholar
  75. Saywitz, K. J., Goodman, G. S., Nicholas, E., & Moan, S. F. (1991). Children's memories of a physical examination involving genital touch: Implications for reports of child sexual abuse.Journal of Consulting and Clinical Psychology, 59 682–691.CrossRefPubMedGoogle Scholar
  76. Schacter, D. (1995). Implicit memory: A new frontier for cognitive neuroscience. In M. S. Gazzaniga (Ed.).The cognitive neurosciences (pp. 815–819). Cambridge, MA: MIT Press.Google Scholar
  77. Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions.Journal of Neurology and Psychiatry, 20 11–21.Google Scholar
  78. Southwick, S. M., Krystal, J. H., Morgan, C. A., Johnson, D., Nagy, L. M., Nicolaou, A., Heninger, G. R., & Charney, D. S. (1993). Abnormal noradrenergic function in posttraumatic stress disorder.Archives of General Psychiatry, 50 266–274.PubMedGoogle Scholar
  79. Spiegel, D., & Cardena, E. (1991). Disintegrated experiences: The dissociative disorders revisited.Journal of Abnormal Psychology, 100 366–378.CrossRefPubMedGoogle Scholar
  80. Squire, L. R., Slater, P. C., & Chace, P. M. (1975). Retrograde amnesia: Temporal gradient in very long term memory following electroconvulsive therapy.Science, 187 77–79.PubMedGoogle Scholar
  81. Squire, L. R., & Zola-Morgan, S. (1991). The medial temporal lobe memory system.Science, 253 1380–1386.PubMedGoogle Scholar
  82. Sutker, P. B., Galina, H., West, J. A., & Allain, A. N. (1990). Trauma-induced weight loss and cognitive deficits among former prisoners of war.American Journal of Psychiatry, 58 323–328.Google Scholar
  83. Sutker, P. B., Winstead, D. K., Galina, Z. H., & Allain, A. N. (1991). Cognitive deficits and psychopathology among former prisoners of war and combat veterans of the Korean conflict.American Journal of Psychiatry, 148 67–72.PubMedGoogle Scholar
  84. Thygesen, P., Hermann, K., & Willanger, R. (1970). Concentration camp survivors in Denmark: Persecution, disease, disability, compensation.Danish Medical Bulletin, 17 65–108.PubMedGoogle Scholar
  85. Torrie, A. (1944). Psychosomatic casualties in the Middle East.Lancet, 29 139–143.CrossRefGoogle Scholar
  86. Tulving, E., Kapur, S., Craik, F. I. M., Moscovitch, M., Houle, S. (1994). Hemispheric encoding/retrieval asymmetry in episodic memory: Positron emission tomography findings.Proceedings of the National Academy of Sciences, USA, 91 2016–2020.Google Scholar
  87. Turner, B. H., & Herkenham, M. (1991). Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing.Journal of Comparative Neurology, 313 295–325.CrossRefPubMedGoogle Scholar
  88. Uddo, M., Vasterling, J. T., Brailey, K., & Sutker, P. B. (1993). Memory and attention in posttraumatic stress disorder.Journal of Psychopathology and Behavioral Assessment, 15 43–52.CrossRefGoogle Scholar
  89. Uno, H., Tarara, R., Else, J. G., Suleman, M. A., & Sapolsky, R. M. (1989). Hippocampal damage associated with prolonged and fatal stress in primates.Journal of Neurosciences, 9 1705–1711.Google Scholar
  90. van der Kolk, B. A., & van der Hart, O. (1989). Pierre Janet and the breakdown of adaptation in psychological trauma.American Journal of Psychiatry, 146 12–17.Google Scholar
  91. van der Kolk, B. A., Dreyfuss, D., Michaels, M., Shera, D., Berkowitz, R., Fisher, R., & Saxe, G. (1994). Fluoxetine in posttraumatic stress disorder.Journal of Clinical Psychiatry, 55 517–522.PubMedGoogle Scholar
  92. Watanabe, Y., Gould, E., & McEwen, B. S. (1992). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons.Brain Research, 588 341–345.CrossRefPubMedGoogle Scholar
  93. Williams, L. M. (1994a). Recall of childhood trauma: A prospective study of women's memories of child sexual abuse.Journal of Consulting and Clinical Psychology, 62 1167–1176.CrossRefPubMedGoogle Scholar
  94. Williams, L. M. (1994b). What does it mean to forget child sexual abuse? A reply to Loftus, Garry, and Feldman (1994).Journal of Consulting and Clinical Psychology, 62 1182–1186.CrossRefGoogle Scholar
  95. Wooley, C. S., Gould, E., & McEwen, B. S. (1990). Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons.Brain Research, 531 225–231.CrossRefPubMedGoogle Scholar
  96. Yehuda, R., Keefer, R. S. E., Harvey, P. D., Levengood, R. A., Gerber, D. K., Geni, J., & Siever, L. J. (1995). Learning and memory in combat veterans with posttraumatic stress disorder.American Journal of Psychiatry, 152 137–139.PubMedGoogle Scholar
  97. Zeitlin, S. B., & McNally, R. J. (1991). Implicit and explicit memory bias for threat in posttraumatic stress disorder.Behavioral Research and Therapeutics, 29 451–457.CrossRefGoogle Scholar
  98. Zola-Morgan, S., Squire, L. R., & Amaral, D. G. (1989): Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation.Journal of Neuroscience, 9 1922–36.PubMedGoogle Scholar
  99. Zola-Morgan, S., Squire, L. R., Amaral, D. G., & Suzuki, W. A. (1989). Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment.Journal of Neuroscience, 9 4355–4370.PubMedGoogle Scholar
  100. Zola-Morgan, S. M., & Squire, L. R. (1990). The primate hippocampal formation: Evidence for a time-limited role in memory storage.Science, 250 288–290.PubMedGoogle Scholar

Copyright information

© International Society for Traumatic Stress Studies 1995

Authors and Affiliations

  • J. Douglas Bremner
    • 1
    • 2
    • 3
  • John H. Krystal
    • 1
    • 2
    • 3
  • Steven M. Southwick
    • 1
    • 2
    • 3
  • Dennis S. Charney
    • 1
    • 2
    • 3
  1. 1.Department of PsychiatryYale University School of MedicineNew Haven
  2. 2.National Center for Posttraumatic Stress Disorder, Division of Clinical NeurosciencesWest Haven
  3. 3.West Haven Veterans Affairs Medical CenterWest Haven

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