Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation (original) (raw)

Abstract

Behavioral stress has detrimental effects on subsequent cognitive performance in many species, including humans. For example, humans exposed to stressful situations typically exhibit marked deficits in various learning and memory tasks. However, the underlying neural mechanisms by which stress exerts its effects on learning and memory are unknown. We now report that in adult male rats, stress (i.e., restraint plus tailshock) impairs long-term potentiation (LTP) but enhances long-term depression (LTD) in the CA1 area of the hippocampus, a structure implicated in learning and memory processes. These effects on LTP and LTD are prevented when the animals were given CGP39551 (the carboxyethylester of CGP 37849; DL-(E)-2-amino-4-methyl-5-phosphono-3-pentenoic acid), a competitive N-methyl-D-aspartate (NMDA) receptor antagonist, before experiencing stress. In contrast, the anxiolytic drug diazepam did not block the stress effects on hippocampal plasticity. Thus, the effects of stress on subsequent LTP and LTD appear to be mediated through the activation of the NMDA subtype of glutamate receptors. Such modifications in hippocampal plasticity may contribute to learning and memory impairments associated with stress.

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Selected References

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  1. Armanini M. P., Hutchins C., Stein B. A., Sapolsky R. M. Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res. 1990 Nov 5;532(1-2):7–12. doi: 10.1016/0006-8993(90)91734-x. [DOI] [PubMed] [Google Scholar]
  2. Bear M. F., Malenka R. C. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol. 1994 Jun;4(3):389–399. doi: 10.1016/0959-4388(94)90101-5. [DOI] [PubMed] [Google Scholar]
  3. Bliss T. V., Collingridge G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993 Jan 7;361(6407):31–39. doi: 10.1038/361031a0. [DOI] [PubMed] [Google Scholar]
  4. Bliss T. V., Gardner-Medwin A. R. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol. 1973 Jul;232(2):357–374. doi: 10.1113/jphysiol.1973.sp010274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bliss T. V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973 Jul;232(2):331–356. doi: 10.1113/jphysiol.1973.sp010273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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. Deficits in short-term memory in posttraumatic stress disorder. Am J Psychiatry. 1993 Jul;150(7):1015–1019. doi: 10.1176/ajp.150.7.1015. [DOI] [PubMed] [Google Scholar]
  7. Collingridge G. L., Kehl S. J., McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol. 1983 Jan;334:33–46. doi: 10.1113/jphysiol.1983.sp014478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Diamond D. M., Fleshner M., Rose G. M. Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav Brain Res. 1994 May 30;62(1):1–9. doi: 10.1016/0166-4328(94)90032-9. [DOI] [PubMed] [Google Scholar]
  9. Diamond D. M., Rose G. M. Stress impairs LTP and hippocampal-dependent memory. Ann N Y Acad Sci. 1994 Nov 30;746:411–414. doi: 10.1111/j.1749-6632.1994.tb39271.x. [DOI] [PubMed] [Google Scholar]
  10. Dudek S. M., Bear M. F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4363–4367. doi: 10.1073/pnas.89.10.4363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Foy M. R., Stanton M. E., Levine S., Thompson R. F. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol. 1987 Jul;48(1):138–149. doi: 10.1016/s0163-1047(87)90664-9. [DOI] [PubMed] [Google Scholar]
  12. Luine V., Villegas M., Martinez C., McEwen B. S. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 1994 Mar 7;639(1):167–170. doi: 10.1016/0006-8993(94)91778-7. [DOI] [PubMed] [Google Scholar]
  13. Maier S. F. Role of fear in mediating shuttle escape learning deficit produced by inescapable shock. J Exp Psychol Anim Behav Process. 1990 Apr;16(2):137–149. [PubMed] [Google Scholar]
  14. Maren S., Baudry M., Thompson R. F. Effects of the novel NMDA receptor antagonist, CGP 39551, on field potentials and the induction and expression of LTP in the dentate gyrus in vivo. Synapse. 1992 Jul;11(3):221–228. doi: 10.1002/syn.890110307. [DOI] [PubMed] [Google Scholar]
  15. Maren S., Tocco G., Standley S., Baudry M., Thompson R. F. Postsynaptic factors in the expression of long-term potentiation (LTP): increased glutamate receptor binding following LTP induction in vivo. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9654–9658. doi: 10.1073/pnas.90.20.9654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Morris R. G., Anderson E., Lynch G. S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. 1986 Feb 27-Mar 5Nature. 319(6056):774–776. doi: 10.1038/319774a0. [DOI] [PubMed] [Google Scholar]
  17. Mulkey R. M., Malenka R. C. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron. 1992 Nov;9(5):967–975. doi: 10.1016/0896-6273(92)90248-c. [DOI] [PubMed] [Google Scholar]
  18. O'Dell T. J., Kandel E. R. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learn Mem. 1994 Jul-Aug;1(2):129–139. [PubMed] [Google Scholar]
  19. Overmier J. B., Seligman M. E. Effects of inescapable shock upon subsequent escape and avoidance responding. J Comp Physiol Psychol. 1967 Feb;63(1):28–33. doi: 10.1037/h0024166. [DOI] [PubMed] [Google Scholar]
  20. SPENCE K. W., TAYLOR J. Anxiety and strength of the UCS as determiners of the amount of eyelid conditioning. J Exp Psychol. 1951 Sep;42(3):183–188. doi: 10.1037/h0061580. [DOI] [PubMed] [Google Scholar]
  21. Seligman M. E., Maier S. F. Failure to escape traumatic shock. J Exp Psychol. 1967 May;74(1):1–9. doi: 10.1037/h0024514. [DOI] [PubMed] [Google Scholar]
  22. Shors T. J., Seib T. B., Levine S., Thompson R. F. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science. 1989 Apr 14;244(4901):224–226. doi: 10.1126/science.2704997. [DOI] [PubMed] [Google Scholar]
  23. Shors T. J., Servatius R. J. Stress-induced sensitization and facilitated learning require NMDA receptor activation. Neuroreport. 1995 Mar 7;6(4):677–680. doi: 10.1097/00001756-199503000-00023. [DOI] [PubMed] [Google Scholar]
  24. Shors T. J., Weiss C., Thompson R. F. Stress-induced facilitation of classical conditioning. Science. 1992 Jul 24;257(5069):537–539. doi: 10.1126/science.1636089. [DOI] [PubMed] [Google Scholar]
  25. Teyler T. J., DiScenna P. Long-term potentiation. Annu Rev Neurosci. 1987;10:131–161. doi: 10.1146/annurev.ne.10.030187.001023. [DOI] [PubMed] [Google Scholar]
  26. Tocco G., Maren S., Shors T. J., Baudry M., Thompson R. F. Long-term potentiation is associated with increased [3H]AMPA binding in rat hippocampus. Brain Res. 1992 Feb 28;573(2):228–234. doi: 10.1016/0006-8993(92)90767-4. [DOI] [PubMed] [Google Scholar]
  27. Tocco G., Shors T. J., Baudry M., Thompson R. F. Selective increase of AMPA binding to the AMPA/quisqualate receptor in the hippocampus in response to acute stress. Brain Res. 1991 Sep 13;559(1):168–171. doi: 10.1016/0006-8993(91)90302-c. [DOI] [PubMed] [Google Scholar]
  28. Watanabe Y., Gould E., McEwen B. S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 1992 Aug 21;588(2):341–345. doi: 10.1016/0006-8993(92)91597-8. [DOI] [PubMed] [Google Scholar]
  29. Woolley C. S., Gould E., McEwen B. S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 1990 Oct 29;531(1-2):225–231. doi: 10.1016/0006-8993(90)90778-a. [DOI] [PubMed] [Google Scholar]