Functional neuroanatomical correlates of the effects of stress on memory

Journal of Traumatic Stress volume 8, pages527–553(1995)Cite this article

Abstract

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.

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References

  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.

    Article  PubMed  Google 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.

    Article  Google Scholar 

  3. Bower, G. H. (1981). Mood and memory.American Psychologist, 36 129–148.

    Article  PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google Scholar 

  13. Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994). Alpha-adrenergic activation and memory for emotional events.Nature, 371 702–703.

    Article  PubMed  Google 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.

    PubMed  Google 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.

    Article  Google Scholar 

  16. Ceci, S. J., & Bruck, M. (1993). Suggestibility of the child witness: A historical review and synthesis.Psychological Bulletin, 113 403–439.

    Article  PubMed  Google 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.

    Article  PubMed  Google Scholar 

  20. Davis, M. (1992). The role of the amygdala in fear and anxiety.Annual Reviews of Neuroscience, 15 353–375.

    Article  Google Scholar 

  21. De Wied, D., & Croiset, G. (1991). Stress modulation of learning and memory processes.Methods and Achievements in Experimental Pathology, 15 167–199.

    PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google Scholar 

  25. Goldman-Rakic, P. S. (1988). Topography of cognition: Parallel distributed networks in primate association cortex.Annual Reviews of Neuroscience, 11 137–156.

    Article  Google Scholar 

  26. Gold, P. E., & van Buskirk, R. (1975). Facilitation of time-dependent memory processes with posttrial epinephrine injections.Behavioral Biology, 13 145–153.

    Article  PubMed  Google 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.

    Article  Google 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.

    PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    PubMed  Google Scholar 

  37. Kihlstrom, J. F., Glisky, M. L., & Angiulo, M. J. (1994). Dissociative tendencies and dissociative disorders.Journal of Abnormal Psychology, 103 117–124.

    Article  PubMed  Google Scholar 

  38. Kim, J. J., & Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear.Science, 256 675–677.

    PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

  42. LeDoux, J. E. (1977). Emotion. InHandbook of physiology-The nervous system V (pp. 419–459).

  43. LeDoux, J. L. (1993). Emotional memory: In search of systems and synapses.Annals of the New York Academy of Sciences, 149–157.

  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.

    Article  PubMed  Google Scholar 

  45. Loftus, E. F., & Loftus, G. R. (1980). On the permanence of stored information in the human brain.American Psychologist, 35 409–420.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    PubMed  Google 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.

    Article  Google 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.

    Article  PubMed  Google 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.

    Article  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google Scholar 

  64. Pitman, R. K. (1989). Posttraumatic stress disorder, hormones, and memory (editorial).Biological Psychiatry, 26 221–223.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    PubMed  Google 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.

  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.

    PubMed  Google Scholar 

  69. Rosen, J. B., & Davis, M. (1988). Enhancement of acoustic startle by electrical stimulation of the amygdala.Behavioral Neuroscience, 102 195–202.

    Article  PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    PubMed  Google Scholar 

  79. Spiegel, D., & Cardena, E. (1991). Disintegrated experiences: The dissociative disorders revisited.Journal of Abnormal Psychology, 100 366–378.

    Article  PubMed  Google 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.

    PubMed  Google Scholar 

  81. Squire, L. R., & Zola-Morgan, S. (1991). The medial temporal lobe memory system.Science, 253 1380–1386.

    PubMed  Google 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.

    PubMed  Google Scholar 

  84. Thygesen, P., Hermann, K., & Willanger, R. (1970). Concentration camp survivors in Denmark: Persecution, disease, disability, compensation.Danish Medical Bulletin, 17 65–108.

    PubMed  Google Scholar 

  85. Torrie, A. (1944). Psychosomatic casualties in the Middle East.Lancet, 29 139–143.

    Article  Google 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.

    Article  PubMed  Google 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.

    Article  Google 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.

    PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  Google 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.

    Article  PubMed  Google 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.

    PubMed  Google 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.

    Article  Google 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.

    PubMed  Google 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.

    PubMed  Google 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.

    PubMed  Google Scholar 

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  1. Department of Psychiatry, Yale University School of Medicine, 06520, New Haven, Connecticut

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

  2. National Center for Posttraumatic Stress Disorder, Division of Clinical Neurosciences, 06516, West Haven, Connecticut

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

  3. West Haven Veterans Affairs Medical Center, 06516, West Haven, Connecticut

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

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Bremner, J.D., Krystal, J.H., Southwick, S.M. et al. Functional neuroanatomical correlates of the effects of stress on memory. J Trauma Stress 8, 527–553 (1995). https://doi.org/10.1007/BF02102888

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Key words

  • PTSD
  • dissociation
  • memory
  • amygdala
  • hippocampus
  • amnesia
  • trauma
  • stress
  • neurobiology