Neurochemical Research

, Volume 28, Issue 11, pp 1735–1742 | Cite as

Stress and Plasticity in the Limbic System

  • Robert M. Sapolsky


The adult nervous system is not static, but instead can change, can be reshaped by experience. Such plasticity has been demonstrated from the most reductive to the most integrated levels, and understanding the bases of this plasticity is a major challenge. It is apparent that stress can alter plasticity in the nervous system, particularly in the limbic system. This paper reviews that subject, concentrating on: a) the ability of severe and/or prolonged stress to impair hippocampal-dependent explicit learning and the plasticity that underlies it; b) the ability of mild and transient stress to facilitate such plasticity; c) the ability of a range of stressors to enhance implicit fear conditioning, and to enhance the amygdaloid plasticity that underlies it.

Stress hippocampus glucocorticoids amygdala LTP LTD 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Sapolsky, R., Romero, M., and Munck, A. 2000. How do glucocorticoids influence the stress-response? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 21: 55-71.PubMedGoogle Scholar
  2. 2.
    Squire, L. 1987 Memory and Brain, New York, Oxford University Press.Google Scholar
  3. 3.
    Conrad, C., Galea, L., Kuroda, Y., and McEwen, B. 1996. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 110:1321-1334.PubMedGoogle Scholar
  4. 4.
    Diamond, D., Park, C., Heman, K., and Rose, G. 1999. Exposing rats to a predator imparis spatial working memory in the radial arm water maze. Hippocampus 9:542-552.PubMedGoogle Scholar
  5. 5.
    Bodnoff, S., Humphreys, A., Lehman, J., Diamond, D., Rose, G., and Meaney, M. 1995. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J. Neurosci. 15:61-69.PubMedGoogle Scholar
  6. 6.
    Bisagno, V., Ferrini, M., Rios, H., Zieher, L., and Wikinski, S. 2000 Chronic corticosterone impairs inhibitory avoidance in rats: Possible link with atrophy of hippocampal CA3 neurons. Pharm. Biochem. Behav. 66:235-240.Google Scholar
  7. 7.
    Endo, Y., Nishimura, J., Kogayashi, S., and Kimura, F. 1999. Chronic stress exposure influences local cerebral blood flow in the rat hippocampus. Neuroscience 93:551-563.PubMedGoogle Scholar
  8. 8.
    Luine, V., Spencer, R., and McEwen, B. 1993. Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Res. 616:65-70.PubMedGoogle Scholar
  9. 9.
    de Quervain, D., Roozendaal, B., and McGaugh, J. 1998. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394:787-790.PubMedGoogle Scholar
  10. 10.
    Roozendaal, B., Griffith, Q., Buranday, J., de Quervain, D., and McGaugh, J. 2003. The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: Dependence upon the basolateral amygdala. Proc. Natl. Acad. Sci. USA 100:1328-1330.PubMedGoogle Scholar
  11. 11.
    Keenan, P., Jacobson, M., Soleymani, R., Mayes, M., Stress, M., and Yaldoo, D. 1996. The effect on memory of chronic prednisone treatment in patients with systemic disease. Neurology 47:1396-1403.PubMedGoogle Scholar
  12. 12.
    Waber, D., Carpentieri, S., Klar, N., Silverman, L., Schwenn, M., Hurwitz, CA., Mullenix, P., Tarbell, N., and Sallan, S. 2000. Cognitive sequelae in children treated for acute lymphoblastic leukemia with dexamethasone or prednisone. J. Ped. Hematol. Oncol. 22:206-215.Google Scholar
  13. 13.
    Starkman, M., Gebarski, S., Berent, S., and Schteingart, D. 1992. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol. Psychiatry 32:756-765.PubMedGoogle Scholar
  14. 14.
    Heuser, I., Schweiger, U., Gotthardt, U., Schmider, J., Lammers, C., Dettling, M., and Holsboer, F. 1996. Pituitary-adrenal system regulation and psycopathology during amitriptyline treatment in elderly depressed patients and normal controls. Am. J. Psychiatry 153: 99-109.Google Scholar
  15. 15.
    Kelly, K., Hayslip, B., and Servaty, H. 1996 Psychoneuroendocrinological indicators of stress and intellectual performance among older adults: An exploratory study. Exp. Aging Res. 22:393-398.PubMedGoogle Scholar
  16. 16.
    Meaney, M., O'Donnell, D., Rowe, W., Tannenbaum, B., Steverman, A., Walker M., Nair, N., and Lupien, S. 1995 Individual differences in HPA activity in later life and hippocampal aging. Exp. Gerontol. 30:229-251.PubMedGoogle Scholar
  17. 17.
    Lupien, S., Lecours, A., Lussier, I., Schwartz, G., Nair, N., and Meaney, M. 1994. Basal cortisol levels and cognitive deficits in human aging. J. Neurosci. 14:2893-2903.PubMedGoogle Scholar
  18. 18.
    Lupien, S. and McEwen, B. 1997. The acute effects of corticosteroids on cognition: Integration of animal and human model studies. Brain Res. Rev. 24:1-27.PubMedGoogle Scholar
  19. 19.
    Lupien, S., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N., Thakur, M., McEwen, B., Hauger, R., and Meaney, M. 1998. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1:69-73.PubMedGoogle Scholar
  20. 20.
    Seeman, T., McEwen, B., Singer, B., Albert, M., and Rowe, J. 1997. Increase in urinary cortisol excretion and memory declines: MacArthur studies of successful aging. J. Clin. Endocrinol. Metab. 82:2458-2467.PubMedGoogle Scholar
  21. 21.
    Sharma, S., Turken, A., Schwartz, G., Nair, N., De Leon, M., Meaney, M., Hauger, R., and Lupien, S. 1995. A longitudinal study of DHEA-S levels, cortisol levels and cognitive function in elderly human subjects. Society of Neuroscience Annual Meeting, Abstract 21.668.Google Scholar
  22. 22.
    Wolkowitz, O., Reuss, V., and Weingartner, H. 1990. Cognitive effects of corticosteroids. Am. J. Psychiatry 147:1297-1310.PubMedGoogle Scholar
  23. 23.
    Wolkowitz, O., Weingartner, H., Rubinow, D., Jimerson, D., Kling, M., Berretini, W., Thompson, K., Breier, A., Doran, A., Reus, V., and Pickar, D. 1993. Steroid modulation of human memory: Biochemical correlates. Biol. Psychiatry 33:744-751.PubMedGoogle Scholar
  24. 24.
    Newcomer, J., Craft, S., Hershey, T., Askins, K., and Bardgett, M. 1994. Glucocorticoid-induced impairment in declarative memory performance in adult human. J. Neurosci. 14:2047-2053.PubMedGoogle Scholar
  25. 25.
    Keenan, P., Jacobson, M., Soleymani, R., and Newcomer, J. 1995. Commonly used therapeutic doses of glucocorticoids impair explicit memory. Ann. NY Acad. Sci. 761:400-402.PubMedGoogle Scholar
  26. 26.
    Newcomer, J., Selke, G., Melson, A., Hershey, T., Craft, S., Richards, K., and Alderson A. 1999. Decreased memory performance in healthy humans induced by stress-level cortisol treatment. Ach. Gen. Psychiatry 56:527-533.Google Scholar
  27. 27.
    Born, J. and Fehm, H. 1999. HPA activity during human sleep: A coordinating role for the limbic hippocampal system. Exp. Clin. Endocrinol. Diabetes 106:153-162.Google Scholar
  28. 28.
    Kirschbaum, C., Wolf, O. T., May, M., Wippich, W., and Hellhammer, D. H. 1996. Stress-and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci. 58:1475-1483.PubMedGoogle Scholar
  29. 29.
    Young, A., Sahakain, B., Robbins, T., and Cowen, P. 1999. The effects of chronic administration of hydrocotisone on cognitive function in normal male volunteers. Psychopharm. 145:260-266.Google Scholar
  30. 30.
    De Quervain, D., Roozendaal, B., Nitsch, R., McGaugh, J., and Hock, C. 2000. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat. Neurosci. 3:313-317.PubMedGoogle Scholar
  31. 31.
    Diamond, D. and Park, C. 2000. Predator exposure produces retrograde amnesia and blocks synaptic plasticity: Progress toward understanding how the hippocampus is affected by stress. Ann. NY Acad. Sci. 911:453-455.PubMedGoogle Scholar
  32. 32.
    Foy, M., Stanton, M., Levine, S. and Thompson, R. 1987. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav. Neural Biol. 48:138-149.PubMedGoogle Scholar
  33. 33.
    Shors, T. and Dryver, E. 1994. Effect of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus. Brain Res. 666:232-238.PubMedGoogle Scholar
  34. 34.
    Shors, T., Seib, T., Levine, S., and Thompson, R. 1989. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244:224-226.PubMedGoogle Scholar
  35. 35.
    Xu, L., Anwyl, R., and Rowan, M. 1997 Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387:497-500.PubMedGoogle Scholar
  36. 36.
    Diamond, D., Fleshner, M., and Rose, G. 1994. Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav. Brain Res. 62:1-9.PubMedGoogle Scholar
  37. 37.
    Diamond, D., Bennett, M., Stevens, K., Wilson, R., and Rose, G. 1990. Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat. Psychobiology 18:273-281.Google Scholar
  38. 38.
    Mesches, M., Fleshner, M., Heman, K., Rose, G., and Diamond, D. 1999. Exposing rats to a predator blocks primed burst potentiation in the hippocampus in vitro. J. Neurosci. 19:RC18.PubMedGoogle Scholar
  39. 39.
    Pavlides, C., Watanabe, Y., Margarinos, A., and McEwen, B. 1995 Opposing roles of type I and type II adrenal steroid receptors in hippocampal long-term potentiation. Neuroscience 68:387-394.PubMedGoogle Scholar
  40. 40.
    Diamond, D., Bennett, M., Engstrom, D., Fleshner, M., and Rose, G. 1989. Adrenalectomy reduces the threshold for hippocampal primed burst potentiation in the anesthetized rat. Brain Res. 492:356-360.PubMedGoogle Scholar
  41. 41.
    Diamond, D. M., Bennett, M. C., Fleshner, M., and Rose, G. M. 1992. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2:421-430.PubMedGoogle Scholar
  42. 42.
    Pavlides, C., Watanabe, Y., and McEwen, B. 1993. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 3:183-192.Google Scholar
  43. 43.
    Zhou, J., Zheng, J., Zhang, Y., Zhou, J. 2000. Corticosterone impairs cultured hippocampal neurons and facilitates Ca2+ influx through voltage-dependent Ca2+ channel. Acta Pharmacol. Sinica 21:156-163.Google Scholar
  44. 44.
    Xu, L., Holscher, C., Anwyl, R., and Rowan, M. J. 1998. Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proc. Natl. Acad. Sci. USA 95:3204-3208.PubMedGoogle Scholar
  45. 45.
    Joels, M. and deKloet, E. 1992. Control of neuronal excitability by corticosteroid hormones. Trends Neurosci. 15:25-30.PubMedGoogle Scholar
  46. 46.
    Kerr, D., Campbell, L., Thibault, O., and Landfield, P. 1992. Hippocampal glucocorticoid receptor activation enhances voltage-dependent calcium conductances: Relevance to brain aging. Proc. Natl. Acad. Sci. USA 89:8527-8531.PubMedGoogle Scholar
  47. 47.
    Hesen, W. and Joels, M. 1993. Modulation of carbachol responsiveness in rat CA1 pyramidal neurons by corticosteroid hormones. Brain Res. 627:157-167.Google Scholar
  48. 48.
    Beck, S., List, T., and Choi, K. 1994. Long and short term administration of corticosterone alters CA1 hippocampal neuronal properties. Neuroendocrinoloogy 60:261-272.Google Scholar
  49. 49.
    Kim, J. J., Foy, M. R., and Thompson, R. F. 1996. Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc. Natl. Acad. Sci. USA 93:4750-4753.PubMedGoogle Scholar
  50. 50.
    Woolley, C., Gould, E., and McEwen, B. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 521:225-31.Google Scholar
  51. 51.
    Watanabe, Y., Gould, E., and McEwen, BS. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588:341-345.PubMedGoogle Scholar
  52. 52.
    Conrad, C. and McEwen, B. 2000. Acute stress increases neuropeptide Y mRNA within the arcuate nucleus and hilus of the dentate gyrus. Mol. Brain Res. 79:102-109.PubMedGoogle Scholar
  53. 53.
    Sunanda, B., Meti, T., and Raju, T. 1997. Entorhinal cortex lesioning protects hippocampal CA3 neurons from stress-induced damage. Brain Res. 770:302-108.Google Scholar
  54. 54.
    Sousa, N., Lukoyanov, N. V., Madeira, M. D., Almeida, O. F., and Paula-Barbosa, M. M. 2000. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97:253-266.PubMedGoogle Scholar
  55. 55.
    Magarinos, A. and McEwen, B. 1995. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69:89-98.PubMedGoogle Scholar
  56. 56.
    Watanabe, Y., Gould, E., Cameron, H., Daniels, D., and McEwen, B. 1992. Phenytoin prevents stress-and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2:431-436.PubMedGoogle Scholar
  57. 57.
    Magarinos, A. and McEwen, B. 1995. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Comparison of stressors. Neuroscience 69:83-88.PubMedGoogle Scholar
  58. 58.
    Czeh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., Bartolomucci, A., and Fuchs, E. 2001. Stress-kinduced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressnat treatment with tianeptine. Proc. Natl. Acad. Sci. USA 98:12796-12801.PubMedGoogle Scholar
  59. 59.
    Luine, V., Villegas, M., Martinez, C., and McEwen, B. 1994. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639:167-170.PubMedGoogle Scholar
  60. 60.
    Magarinos, A., McEwen, B., Flugge, D., and Fuchs, E. 1996. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J. Neurosci. 16:3534-3540.PubMedGoogle Scholar
  61. 61.
    Starkman, M., Giordani, B., Gebarski, S., Berent, S., Schork, M., and Schteingart, D. 1999. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol. Psychiatry 46:1595-1602.PubMedGoogle Scholar
  62. 62.
    Gould, E. and Gross, C. 2002. Neurogenesis in adult mammals: Some progress and problems. J. Neurosci. 22:619-623.PubMedGoogle Scholar
  63. 63.
    Van Praag, H., Schinder, A., Christie, B., Toni, N., Palmer, T., and Gage, F. 2002. Functional neurogenssis in the adult hippocampus. Nature 415:1030-1034.PubMedGoogle Scholar
  64. 64.
    Shors, T., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., and Gould, E. 2001. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.PubMedGoogle Scholar
  65. 65.
    Sapolsky, R. 1999. Stress, glucocorticoids and their adverse neurological effects: Relevance to aging. Exp. Gerontol. 34: 721-735.PubMedGoogle Scholar
  66. 66.
    Landfield, P., Baskin, R., and Pitler, T. 1981. Brain-aging correlates: Retardation by hormonal-pharmacological treatments. Science 214:581-584.PubMedGoogle Scholar
  67. 67.
    Sapolsky, R., Krey, L., and McEwen, B. 1985. Prolonged glucocorticoid exposure reduces hippocampal neuron number: Implications for aging. J. Neurosci. 5:1221-1227.Google Scholar
  68. 68.
    Kerr, D., Campbell, L., Applegate, M., Brodish, A., and Landfield, P. 1991. Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J. Neurosci. 11:1316-1322.PubMedGoogle Scholar
  69. 69.
    McEwen, B. 1999. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22:105-122.PubMedGoogle Scholar
  70. 70.
    Piazza, P. and Le Moal, M. 1997. Glucocortiocids as a biological substrate of reward: Physiological and pathophysiological implications. Brain Res. Rev. 25:359-378.PubMedGoogle Scholar
  71. 71.
    Kim, J. and Diamond, D. 2002. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3:4534-4562.Google Scholar
  72. 72.
    Luine, V., Martinez, C., Villegas, M., Magarinos, A., and McEwen, B. 1996. Restraint stress reversibly enhances spatial memory performance. Physiol. Behav. 59:27-32.PubMedGoogle Scholar
  73. 73.
    Luine, V. 2002. Sex differences in chronic stress effects on memory in rats. Stress 5:205-216.PubMedGoogle Scholar
  74. 74.
    Beck, K. and Luine, V. 1999. Food deprivation modulates chronic stress effects on object recognition in male rats: Role of monoamines and amino acid. Brain Res. 830:56-71.PubMedGoogle Scholar
  75. 75.
    McLay, R., Freeman, S., and Zadina, J. 1998. Chronic corticosterone impairs memory performance in the Barnes maze. Physiol. Behav. 63:933-7.PubMedGoogle Scholar
  76. 76.
    Tabira, T. 2000. Chronic stress induces impairment of spatial working memory and of prefrontal dopaminergic dysfunction. J. Neurosci. 20:1568-1574.PubMedGoogle Scholar
  77. 77.
    Sandi, C., Loscertales, M., and Guanza, C. 1997. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 9:637-642.PubMedGoogle Scholar
  78. 78.
    Conrad, C., LeDoux, J., Magarinos, A., and McEwen, B. 1999. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 113:902-913.PubMedGoogle Scholar
  79. 79.
    Joels, M. 2001. Corticosteroid actions in the hippocampus. J. Neuroendocrinol. 13:657-669.PubMedGoogle Scholar
  80. 80.
    Pavlides, C., Kimura, A., Magarinos, A., and McEwen, B. 1994. Type I adrenal steroid receptors prolong hippocampal long-term potentiation. Neuroreport 5:2673-2677.PubMedGoogle Scholar
  81. 81.
    Vaher, P., Luine, V., Gould, E., and McEwen, B. 1994 Effects of adrenalectomy on spatial memory performance and dentate gyrus morphology. Brain Res. 656:71-78.PubMedGoogle Scholar
  82. 82.
    Oitzl, M., Fluttert, M., and de Kloet, E. 1998. Acute blockade of hippocmapal glucocorticoid receptors facilitates spatial learning in rats. Brain Res. 797:159-166.PubMedGoogle Scholar
  83. 83.
    Conrad, C., LeDoux, J., Magarinos, A., and McEwen, B. 1999. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 113:902-913.PubMedGoogle Scholar
  84. 84.
    Oiztl, M. and de Kloet, E. 1992. Selective corticosteriod antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106:62-71.PubMedGoogle Scholar
  85. 85.
    Roozendaal, B., Portillo-Marquez, G., and McGaugh, J. 1996. Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav. Neurosci. 100:1074-1083.Google Scholar
  86. 86.
    De Kloet, E., de Kock, S., Schild, V., and Veldhuis, H. 1988. Antiglucocorticoid RU 38486 attenuates retention of a behavior and disinhibits the hypothalamic-pituitary-adrenal axis at different sites. Neuroendocrinology 47:109-115.PubMedGoogle Scholar
  87. 87.
    Korte, S., de Kloet, E., Buwalda, B., Bopuman, S., and Bohus, B. 1996. Antisense to the glucocorticoid receptor in hippocampal dentate gyrus reduces immobility in forced swim test. Eur. J. Pharmacol. 301:19-25.PubMedGoogle Scholar
  88. 88.
    Shors, T., Weiss, C., and Thompson, R. 1992. Stress-induced facilitation of classical conditioning. Science 257:537-539.PubMedGoogle Scholar
  89. 89.
    Shors, T., Chua, C., and Falduto, J. 2001. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J. Neurosci. 21:6292-6297.PubMedGoogle Scholar
  90. 90.
    Servatius, R., and Shors, T. 1994. Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav. Neurosci. 108:1101-1106.PubMedGoogle Scholar
  91. 91.
    Korte, S. 2001. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci. Biobehav. Rev. 25:117-131.PubMedGoogle Scholar
  92. 92.
    LeDoux, J. 2000. Emotion circuits in the brain. Annu. Rev. Neurosci. 23:155-184.PubMedGoogle Scholar
  93. 93.
    Vyas, A., Mitra, R., Shankaranarayana Rao, B., and Chatterji, S. 2002. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 22:6810-6818.PubMedGoogle Scholar
  94. 94.
    Vyas, A., Bernal, S., and Chattarji, S. 2003. Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res. 965:290-294.PubMedGoogle Scholar
  95. 95.
    Roozendaal, B. 2000. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25:213-238.PubMedGoogle Scholar
  96. 96.
    Dolan, R. 2002. Emotion, cognition and behavior. Science 298:1191-1197.PubMedGoogle Scholar
  97. 97.
    Cahill, L., Prins, B., Weber, M., and McGaugh, J. 1994. Beta-adrenergifc activation and memory for emotional events. Nature 371:702-704.PubMedGoogle Scholar
  98. 98.
    McGaugh, J. 2003. Emotion and Memory. New York, Weidenfeld and Nicolson.Google Scholar
  99. 99.
    Galea, S., Resnick, H., Ahern, J., Gold, J., Bucuvalas, M., Kilpatrick, D., Stuber, J., and Vlahov, D. 2002. PTSD in Manhattan, New York City, after the September 11th terrorist attacks. J. Urban Health Bull. N Y Acad. Med. 79:340-353.Google Scholar
  100. 100.
    Schlenger, W., Caddell, J., Ebert, L., Jordan, B., Rourke, K., Wilson, D., Thalji, L., Dennis, J., Fairbank, J., and Kulka, R. 2002. Psychological reactions to terrorist attacks: Findings from the National Study of Americans' Reactions to September 11. JAMA 288:581-588.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 2003

Authors and Affiliations

  • Robert M. Sapolsky
    • 1
  1. 1.Departments of Biological Sciences, and of Neurology and Neurological SciencesStanford University, Gilbert LaboratoryStanford

Personalised recommendations