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Neural Plasticity
Volume 2007 (2007), Article ID 93202, 6 pages
http://dx.doi.org/10.1155/2007/93202
Review Article

LTP after Stress: Up or Down?

SILS-CNS, University of Amsterdam, SM Amsterdam 1098, The Netherlands

Received 4 September 2006; Revised 4 January 2007; Accepted 6 January 2007

Academic Editor: Benno Roozendaal

Copyright © 2007 Marian Joëls and Harm J. Krugers. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. R. de Kloet, M. Joëls, and F. Holsboer, “Stress and the brain: from adaptation to disease,” Nature Reviews Neuroscience, vol. 6, no. 6, pp. 463–475, 2005. View at Publisher · View at Google Scholar · View at PubMed
  2. J. M. H. M. Reul and E. R. de Kloet, “Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation,” Endocrinology, vol. 117, no. 6, pp. 2505–2511, 1985.
  3. B. S. McEwen, E. R. de Kloet, and W. Rostene, “Adrenal steroid receptors and actions in the nervous system,” Physiological Reviews, vol. 66, no. 4, pp. 1121–1188, 1986.
  4. H. Gronemeyer, J.-Å. Gustafsson, and V. Laudet, “Principles for modulation of the nuclear receptor superfamily,” Nature Reviews Drug Discovery, vol. 3, no. 11, pp. 950–964, 2004. View at Publisher · View at Google Scholar · View at PubMed
  5. B. S. McEwen, J. M. Weiss, and L. S. Schwartz, “Selective retention of corticosterone by limbic structures in rat brain,” Nature, vol. 220, no. 170, pp. 911–912, 1968. View at Publisher · View at Google Scholar
  6. T. V. P. Bliss and T. Lomo, “Long lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path,” Journal of Physiology, vol. 232, no. 2, pp. 331–356, 1973.
  7. R. G. M. Morris, E. Anderson, G. S. Lynch, and M. Baudry, “Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5,” Nature, vol. 319, no. 6056, pp. 774–776, 1986. View at Publisher · View at Google Scholar · View at PubMed
  8. M. R. Foy, M. E. Stanton, S. Levine, and R. F. Thompson, “Behavioral stress impairs long-term potentiation in rodent hippocampus,” Behavioral and Neural Biology, vol. 48, no. 1, pp. 138–149, 1987. View at Publisher · View at Google Scholar
  9. T. J. Shors, T. B. Seib, S. Levine, and R. F. Thompson, “Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus,” Science, vol. 244, no. 4901, pp. 224–226, 1989. View at Publisher · View at Google Scholar
  10. M. H. Mesches, M. Fleshner, K. L. Heman, G. M. Rose, and D. M. Diamond, “Exposing rats to a predator blocks primed burst potentiation in the hippocampus in vitro,” The Journal of Neuroscience, vol. 19, no. 14, p. RC18, 1999.
  11. J. J. Kim, M. R. Foy, and R. F. Thompson, “Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 10, pp. 4750–4753, 1996. View at Publisher · View at Google Scholar
  12. D. N. Alfarez, O. Wiegert, M. Joëls, and H. J. Krugers, “Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation,” Neuroscience, vol. 115, no. 4, pp. 1119–1126, 2002. View at Publisher · View at Google Scholar
  13. C.-H. Yang, C.-C. Huang, and K.-S. Hsu, “Behavioral stress modifies hippocampal synaptic plasticity through corticosterone-induced sustained extracellular signal-regulated kinase/mitogen-activated protein kinase activation,” The Journal of Neuroscience, vol. 24, no. 49, pp. 11029–11034, 2004. View at Publisher · View at Google Scholar · View at PubMed
  14. C. Pavlides, A. Kimura, A. M. Magarinos, and B. S. McEwen, “Hippocampal homosynaptic long-term depression/depotentiation induced by adrenal steroids,” Neuroscience, vol. 68, no. 2, pp. 379–385, 1995. View at Publisher · View at Google Scholar
  15. L. Xu, R. Anwyl, and M. J. Rowan, “Behavioural stress facilitates the induction of long-term depression in the hippocampus,” Nature, vol. 387, no. 6632, pp. 497–500, 1997. View at Publisher · View at Google Scholar · View at PubMed
  16. L. Xu, C. Holscher, R. Anwyl, and M. J. Rowan, “Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 6, pp. 3204–3208, 1998. View at Publisher · View at Google Scholar
  17. D. M. Diamond, M. C. Bennett, M. Fleshner, and G. M. Rose, “Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation,” Hippocampus, vol. 2, no. 4, pp. 421–430, 1992. View at Publisher · View at Google Scholar · View at PubMed
  18. C. Pavlides, S. Ogawa, A. Kimura, and B. S. McEwen, “Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices,” Brain research, vol. 738, no. 2, pp. 229–235, 1996. View at Publisher · View at Google Scholar
  19. M. Joëls and E. R. de Kloet, “Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems,” Progress in Neurobiology, vol. 43, no. 1, pp. 1–36, 1994. View at Publisher · View at Google Scholar
  20. M. Joëls, “Corticosteroid effects in the brain: U-shape it,” Trends in Pharmacological Sciences, vol. 27, no. 5, pp. 244–250, 2006. View at Publisher · View at Google Scholar · View at PubMed
  21. J. J. Kim, H. J. Lee, J.-S. Han, and M. G. Packard, “Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning,” The Journal of Neuroscience, vol. 21, no. 14, pp. 5222–5228, 2001.
  22. J. J. Kim, J. W. Koo, H. J. Lee, and J.-S. Han, “Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory,” The Journal of Neuroscience, vol. 25, no. 6, pp. 1532–1539, 2005. View at Publisher · View at Google Scholar · View at PubMed
  23. M. Joëls and E. R. de Kloet, “Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus,” Science, vol. 245, no. 4925, pp. 1502–1505, 1989.
  24. D. S. Kerr, L. W. Campbell, S.-Y. Hao, and P. W. Landfield, “Corticosteroid modulation of hippocampal potentials: increased effect with aging,” Science, vol. 245, no. 4925, pp. 1505–1509, 1989. View at Publisher · View at Google Scholar
  25. C. Weiss, E. Sametsky, A. Sasse, J. Spiess, and J. F. Disterhoft, “Acute stress facilitates trace eyeblink conditioning in C57BL/6 male mice and increases the excitability of their CA1 pyramidal neurons,” Learning and Memory, vol. 12, no. 2, pp. 138–143, 2005. View at Publisher · View at Google Scholar · View at PubMed
  26. D. S. Kerr, L. W. Campbell, O. Thibault, and P. W. Landfield, “Hippocampal glucocorticoid receptor activation enhances voltage-dependent Ca2+ conductances: relevance to brain aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 18, pp. 8527–8531, 1992. View at Publisher · View at Google Scholar
  27. H. Karst, Y. J. G. Karten, H. M. Reichardt, E. R. de Kloet, G. Schütz, and M. Joëls, “Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers,” Nature Neuroscience, vol. 3, no. 10, pp. 977–978, 2000. View at Publisher · View at Google Scholar · View at PubMed
  28. D. M. Diamond, C. R. Park, A. M. Campbell, and J. C. Woodson, “Competitive interactions between endogenous LTD and LTP in the hippocampus underlie the storage of emotional memories and stress-induced amnesia,” Hippocampus, vol. 15, no. 8, pp. 1006–1025, 2005. View at Publisher · View at Google Scholar · View at PubMed
  29. H. Karst and M. Joëls, “Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells,” Journal of Neurophysiology, vol. 94, no. 5, pp. 3479–3486, 2005. View at Publisher · View at Google Scholar · View at PubMed
  30. P. Sah and J. M. Bekkers, “Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation,” The Journal of Neuroscience, vol. 16, no. 15, pp. 4537–4542, 1996.
  31. C. M. Norris, S. Halpain, and T. C. Foster, “Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels,” The Journal of Neuroscience, vol. 18, no. 9, pp. 3171–3179, 1998.
  32. J. Kim and K. S. Yoon, “Stress: metaplastic effects in the hippocampus,” Trends in Neurosciences, vol. 21, no. 12, pp. 505–509, 1998. View at Publisher · View at Google Scholar
  33. P. K. Stanton and J. M. Sarvey, “Norepinephrine regulates long-term potentiation of both the population spike and dendritic EPSP in hippocampal dentate gyrus,” Brain Research Bulletin, vol. 18, no. 1, pp. 115–119, 1987. View at Publisher · View at Google Scholar
  34. T. Blank, I. Nijholt, K. Eckart, and J. Spiess, “Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning,” The Journal of Neuroscience, vol. 22, no. 9, pp. 3788–3794, 2002.
  35. O. Wiegert, Z. Pu, S. Shor, M. Joëls, and H. J. Krugers, “Glucocorticoid receptor activation selectively hampers N-methyl-D-aspartate receptor dependent hippocampal synaptic plasticity in vitro,” Neuroscience, vol. 135, no. 2, pp. 403–411, 2005. View at Publisher · View at Google Scholar · View at PubMed
  36. H. J. Krugers, D. N. Alfarez, H. Karst, K. Parashkouhi, N. van Gemert, and M. Joëls, “Corticosterone shifts different forms of synaptic potentiation in opposite directions,” Hippocampus, vol. 15, no. 6, pp. 697–703, 2005. View at Publisher · View at Google Scholar · View at PubMed
  37. E. P. Bauer, G. E. Schafe, and J. E. LeDoux, “NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala,” The Journal of Neuroscience, vol. 22, no. 12, pp. 5239–5249, 2002.
  38. C. Pavlides, Y. Watanabe, and B. S. McEwen, “Effects of glucocorticolds on hippocampal long-term potentiation,” Hippocampus, vol. 3, no. 2, pp. 183–192, 1993. View at Publisher · View at Google Scholar · View at PubMed
  39. T. J. Shors and E. Dryver, “Effect of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus,” Brain Research, vol. 666, no. 2, pp. 232–238, 1994. View at Publisher · View at Google Scholar
  40. C. R. Bramham, T. Southard, S. T. Ahlers, and J. M. Sarvey, “Acute cold stress leading to elevated corticosterone neither enhances synaptic efficacy nor impairs LTP in the dentate gyrus of freely moving rats,” Brain Research, vol. 789, no. 2, pp. 245–255, 1998. View at Publisher · View at Google Scholar
  41. N. Z. Gerges, J. L. Stringer, and K. A. Alkadhi, “Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats,” Brain Research, vol. 922, no. 2, pp. 250–260, 2001. View at Publisher · View at Google Scholar
  42. D. N. Alfarez, M. Joëls, and H. J. Krugers, “Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro,” European Journal of Neuroscience, vol. 17, no. 9, pp. 1928–1934, 2003. View at Publisher · View at Google Scholar
  43. A. Kavushansky, R.-M. Vouimba, H. Cohen, and G. Richter-Levin, “Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress,” Hippocampus, vol. 16, no. 1, pp. 35–42, 2006. View at Publisher · View at Google Scholar · View at PubMed
  44. I. Akirav and G. Richter-Levin, “Mechanisms of amygdala modulation of hippocampal plasticity,” The Journal of Neuroscience, vol. 22, no. 22, pp. 9912–9921, 2002.
  45. K. Nakao, K. Matsuyama, N. Matsuki, and Y. Ikegaya, “Amygdala stimulation modulates hippocampal synaptic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 39, pp. 14270–14275, 2004. View at Publisher · View at Google Scholar · View at PubMed
  46. H. Karst, S. Berger, M. Turiault, F. Tronche, G. Schütz, and M. Joëls, “Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 52, pp. 19204–19207, 2005. View at Publisher · View at Google Scholar · View at PubMed
  47. C. Venero and J. Borrell, “Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats,” European Journal of Neuroscience, vol. 11, no. 7, pp. 2465–2473, 1999. View at Publisher · View at Google Scholar
  48. O. Wiegert, M. Joëls, and H. J. Krugers, “Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus,” Learning and Memory, vol. 13, no. 2, pp. 110–113, 2006. View at Publisher · View at Google Scholar · View at PubMed
  49. V. Korz and J. U. Frey, “Stress-related modulation of hippocampal long-term potentiation in rats: involvement of adrenal steroid receptors,” The Journal of Neuroscience, vol. 23, no. 19, pp. 7281–7287, 2003.
  50. C. Pavlides, L. G. Nivón, and B. S. McEwen, “Effects of chronic stress on hippocampal long-term potentiation,” Hippocampus, vol. 12, no. 2, pp. 245–257, 2002. View at Publisher · View at Google Scholar · View at PubMed
  51. D. L. Champagne, E. R. de Kloet, M. Meaney, M. Joëls, and H. J. Krugers, “Maternal care and hippocampal plasticity,” in Proceedings of the 5th Forum of European Neuroscience (FENS '06), vol. 3, Vienna, Austria, July 2006, Abstract A230.4.
  52. J. Grootendorst, M. Kempes, P. Lucassen, S. Dalm, E. R. de Kloet, and M. S. Oitzl, “Differential effect of corticosterone on spatial learning abilities in apolipoprotein E knockout and C57BL/6J mice,” Brain Research, vol. 953, no. 1-2, pp. 281–285, 2002. View at Publisher · View at Google Scholar
  53. E. R. de Kloet, M. S. Oitzl, and M. Joëls, “Stress and cognition: are corticosteroids good or bad guys?,” Trends in Neurosciences, vol. 22, no. 10, pp. 422–426, 1999. View at Publisher · View at Google Scholar
  54. J. L. McGaugh, “The amygdala modulates the consolidation of memories of emotionally arousing experiences,” Annual Review of Neuroscience, vol. 27, pp. 1–28, 2004. View at Publisher · View at Google Scholar · View at PubMed
  55. M. A. Lynch, “Long-term potentiation and memory,” Physiological Reviews, vol. 84, no. 1, pp. 87–136, 2004. View at Publisher · View at Google Scholar · View at PubMed
  56. C. K. McIntyre, T. Hatfield, and J. L. McGaugh, “Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats,” European Journal of Neuroscience, vol. 16, no. 7, pp. 1223–1226, 2002. View at Publisher · View at Google Scholar
  57. B. Roozendaal and J. L. McGaugh, “Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage,” Neurobiology of Learning and Memory, vol. 67, no. 2, pp. 176–179, 1997. View at Publisher · View at Google Scholar · View at PubMed
  58. M. S. Oitzl and E. R. de Kloet, “Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning,” Behavioral Neuroscience, vol. 106, no. 1, pp. 62–71, 1992. View at Publisher · View at Google Scholar
  59. C. Sandi, M. Loscertales, and C. Guaza, “Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze,” European Journal of Neuroscience, vol. 9, no. 4, pp. 637–642, 1997. View at Publisher · View at Google Scholar
  60. B. Roozendaal, S. Okuda, E. A. van der Zee, and J. L. McGaugh, “Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 17, pp. 6741–6746, 2006. View at Publisher · View at Google Scholar · View at PubMed
  61. D. J.-F. De Quervain, “Glucocorticoid-induced inhibition of memory retrieval: implications for posttraumatic stress disorder,” Annals of the New York Academy of Sciences, vol. 1071, pp. 216–220, 2006. View at Publisher · View at Google Scholar · View at PubMed
  62. M. S. Oitzl, H. M. Reichardt, M. Joëls, and E. R. de Kloet, “Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 22, pp. 12790–12795, 2001. View at Publisher · View at Google Scholar · View at PubMed
  63. S. J. Lupien, A. Fiocco, and N. Wan et al., “Stress hormones and human memory function across the lifespan,” Psychoneuroendocrinology, vol. 30, no. 3, pp. 225–242, 2005. View at Publisher · View at Google Scholar · View at PubMed
  64. R. Yehuda, “Biology of posttraumatic stress disorder,” Journal of Clinical Psychiatry, vol. 62, supplement 17, pp. 41–46, 2001.
  65. J. R. Whitlock, A. J. Heynen, M. G. Shuler, and M. F. Bear, “Learning induces long-term potentiation in the hippocampus,” Science, vol. 313, no. 5790, pp. 1093–1097, 2006. View at Publisher · View at Google Scholar · View at PubMed