Psychological stress impairs spatial working memory: Relevance to electrophysiological studies of hippocampal function.

Diamond, David M., Fleshner, Monika, Ingersoll, Nan, Rose, Gregory M.·1996·Behavioral Neuroscience

Abstract

Stress blocks hippocampal primed-burst potentiation, a low threshold form of long-term potentiation, thereby suggesting that stress should also impair hippocampal-dependent memory. Therefore, the effects of stress on working (hippocampal-dependent) and reference (hippocampal-independent) memory were evaluated. Rats foraged for food in seven arms of a 14-arm radial maze. After they ate the food in four of the seven baited arms, they were placed in an unfamiliar environment (stress) for a 4-hr delay. At the end of the delay they were returned to the maze to locate the food in the 3 remaining baited arms. Stress impaired only working memory. Stress interfered with the retrieval of previously stored information (retrograde amnesia), but did not produce anterograde amnesia. Stress appears to induce a transient disruption of hippocampal function, which is revealed behaviorally as retrograde amnesia and physiologically as a blockade of synaptic plasticity.

Cites (6)

  1. The Medial Temporal Lobe Memory System
    Squire, Larry R., Zola-Morgan, Stuart · 1991 · Science
  2. Failure to escape traumatic shock.
    Seligman, Martin E., Maier, Steven F. · 1967 · Journal of Experimental Psychology
  3. β-Adrenergic activation and memory for emotional events
    Cahill, Larry, Prins, Bruce, Weber, Michael, McGaugh, James L. · 1994 · Nature
  4. Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus
    Stein-Behrens, B, Mattson, MP, Chang, I, Yeh, M, Sapolsky, R · 1994 · The Journal of Neuroscience
  5. Effects of glucocorticoids on hippocampal long‐term potentiation
    Pavlides, Constantine, Watanabe, Yoshifumi, McEwen, Bruce S. · 1993 · Hippocampus
  6. Acute stress impairs (or induces) synaptic long‐term potentiation (LTP) but does not affect paired‐pulse facilitation in the stratum radiatum of rat hippocampus
    Shors, Tracey J., Thompson, Richard F. · 1992 · Synapse

Cited by (33)

  1. Child abuse: Adolescent records vs. adult recall
    Femina, Donna Della, Yeager, Catherine A., Lewis, Dorothy Otnow · 1990 · Child Abuse & Neglect
  2. The enduring effects of abuse and related adverse experiences in childhood: A convergence of evidence from neurobiology and epidemiology
    Anda, R. F., Felitti, V. J., Bremner, J. D., Walker, J. D., Whitfield, Ch., Perry, B. D., Dube, Sh. R., Giles, W. H. · 2006 · European archives of psychiatry and clinical neuroscience
  3. Brain corticosteroid receptor balance in health and disease
    de Kloet, E. Ronald, Vreugdenhil, Erno, Oitzl, Melly S., Joëls, Marian · 1998 · Endocrine Reviews
  4. The neurobiology of stress: from serendipity to clinical relevance11Published on the World Wide Web on 22 November 2000.
    McEwen, Bruce S. · 2000 · Brain Research
  5. Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress
    Charney, Dennis S. · 2004 · American Journal of Psychiatry
  6. The stressed hippocampus, synaptic plasticity and lost memories
    Kim, Jeansok J., Diamond, David M. · 2002 · Nature Reviews Neuroscience
  7. The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law
    Diamond, David M., Campbell, Adam M., Park, Collin R., Halonen, Joshua, Zoladz, Phillip R. · 2007 · Neural Plasticity
  8. Sex, stress and the hippocampus: allostasis, allostatic load and the aging process
    MCEWEN, B · 2002 · Neurobiology of Aging
  9. Traumatic stress: effects on the brain
    Bremner, J. Douglas · 2006 · Dialogues in Clinical Neuroscience
  10. Effects of adverse experiences for brain structure and function
    McEwen, Bruce S · 2000 · Biological Psychiatry
  11. Stress and memory in humans: twelve years of progress?
    Wolf, Oliver T. · 2009 · Brain Research
  12. Chronic Stress-induced Hippocampal Vulnerability: The Glucocorticoid Vulnerability Hypothesis
    Conrad, Cheryl D. · 2008 · Reviews in the Neurosciences
  13. Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: a meta-analysis
    Kitayama, Noriyuki, Vaccarino, Viola, Kutner, Michael, Weiss, Paul, Bremner, J. Douglas · 2005 · Journal of Affective Disorders
  14. Glucocorticoid effects on object recognition memory require training-associated emotional arousal
    Okuda, Shoki, Roozendaal, Benno, McGaugh, James L. · 2004 · Proceedings of the National Academy of Sciences
  15. The relationship between stress induced cortisol levels and memory differs between men and women
    Wolf, Oliver T., Schommer, Nicole C., Hellhammer, Dirk H., McEwen, Bruce S., Kirschbaum, C. · 2001 · Psychoneuroendocrinology
  16. Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders
    McEwen, Bruce S., Magarinos, Ana Maria · 2001 · Human Psychopharmacology: Clinical and Experimental
  17. Exposing Rats to a Predator Blocks Primed Burst Potentiation in the Hippocampus<i>In Vitro</i>
    Mesches, Michael H., Fleshner, Monika, Heman, Karen L., Rose, Gregory M., Diamond, David M. · 1999 · The Journal of Neuroscience
  18. Possible mechanisms for atrophy of the human hippocampus
    McEwen, B S · 1997 · Molecular Psychiatry
  19. Long-term effects of childhood abuse on brain and neurobiology
    Bremner, J.Douglas · 2003 · Child and Adolescent Psychiatric Clinics of North America
  20. Protective effects of idebenone and α‐tocopherol on β‐amyloid‐(1–42)‐induced learning and memory deficits in rats: implication of oxidative stress in β‐amyloid‐induced neurotoxicity in vivo
    Yamada, Kiyofumi, Tanaka, Tomoko, Han, Daiken, Senzaki, Kouji, Kameyama, Tsutomu, Nabeshima, Toshitaka · 1999 · European Journal of Neuroscience
  21. Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze
    Dong, Zhifang, Bai, Yanrui, Wu, Xiaoyan, Li, Hongjie, Gong, Bo, Howland, John G., Huang, Yan, He, Wenting, Li, Tingyu, Wang, Yu Tian · 2013 · Neuropharmacology
  22. Circadian regulation of cortisol after hippocampal damage in humans
    Buchanan, Tony W., Kern, Simone, Allen, John S., Tranel, Daniel, Kirschbaum, Clemens · 2004 · Biological Psychiatry
  23. Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala
    Johnson, L.R., Farb, C., Morrison, J.H., McEwen, B.S., Ledoux, J.E. · 2005 · Neuroscience
  24. Deficits in hippocampal and anterior cingulate functioning during verbal declarative memory encoding in midlife major depression
    Bremner, J. Douglas, Vythilingam, Meena, Vermetten, Eric, Vaccarino, Viola, Charney, Dennis S. · 2004 · American Journal of Psychiatry
  25. The neurobiology and neuroendocrinology of stress
    McEwen, Bruce S · 2002 · Psychiatric Clinics of North America
  26. Overcoming the effects of stress on synaptic plasticity in the intact hippocampus: rapid actions of serotonergic and antidepressant agents
    Shakesby, Alison C., Anwyl, Roger, Rowan, Michael J. · 2002 · The Journal of Neuroscience
  27. Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress
    Yang, Jianli, Hou, Cailan, Ma, Ning, Liu, Jun, Zhang, Yan, Zhou, Jiansong, Xu, Lin, Li, Lingjiang · 2007 · Neurobiology of Learning and Memory
  28. Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex
    Sandi, Carmen, Woodson, James C., Haynes, Vernon F., Park, Collin R., Touyarot, Katia, Lopez-Fernandez, Miguel A., Venero, César, Diamond, David M. · 2005 · Biological Psychiatry
  29. REM sleep deprivation-induced deficits in the latency-to-peak induction and maintenance of long-term potentiation within the CA1 region of the hippocampus
    Davis, Christopher J., Harding, Joseph W., Wright, John W. · 2003 · Brain Research
  30. Differential effects of predator stress and the antidepressant tianeptine on physiological plasticity in the hippocampus and basolateral amygdala
    Vouimba, Rose-Marie, Muñoz, Carmen, Diamond, David M. · 2006 · Stress
  31. Stress generates emotional memories and retrograde amnesia by inducing an endogenous form of hippocampal LTP
    Diamond, David M., Park, Collin R., Woodson, James C. · 2004 · Hippocampus
  32. Enhancement of striatum-dependent memory by conditioned fear is mediated by beta-adrenergic receptors in the basolateral amygdala
    Goode, Travis D., Leong, Kah-Chung, Goodman, Jarid, Maren, Stephen, Packard, Mark G. · 2016 · Neurobiology of Stress
  33. Impaired memory following predatory stress in mice is improved by fluoxetine
    El Hage, Wissam, Peronny, Sylvie, Griebel, Guy, Belzung, Catherine · 2004 · Progress in Neuro-Psychopharmacology and Biological Psychiatry