LTP after Stress: Up or Down?

Joëls, Marian; Krugers, Harm J.

doi:https://doi.org/10.1155/2007/93202

Neural Plasticity

On this page

Abstract References Copyright Related Articles

Review Article | Open Access

Volume 2007 | Article ID 093202 | https://doi.org/10.1155/2007/93202

LTP after Stress: Up or Down?

Marian Joëls¹and Harm J. Krugers¹

Academic Editor: Benno Roozendaal

Received04 Sept 2006

Revised04 Jan 2007

Accepted06 Jan 2007

Published13 Mar 2007

Abstract

When an organism is exposed to a stressful situation, corticosteroid levels in the brain rise. This rise has consequences for behavioral performance, including memory formation. Over the past decades, it has become clear that a rise in corticosteroid level is also accompanied by a reduction in hippocampal long-term potentiation (LTP). Recent studies, however, indicate that stress does not lead to a universal suppression of LTP. Many factors, including the type of stress, the phase of the stress response, the area of investigation, type of LTP, and the life history of the organism determine in which direction LTP will be changed.

References

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 Site | Google Scholar
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.
View at: Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
D. S. Kerr, L. W. Campbell, O. Thibault, and P. W. Landfield, “Hippocampal glucocorticoid receptor activation enhances voltage-dependent ${Ca}^{2 +}$ 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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
C. M. Norris, S. Halpain, and T. C. Foster, “Reversal of age-related alterations in synaptic plasticity by blockade of L-type ${Ca}^{2 +}$ channels,” The Journal of Neuroscience, vol. 18, no. 9, pp. 3171–3179, 1998.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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.
View at: Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
M. A. Lynch, “Long-term potentiation and memory,” Physiological Reviews, vol. 84, no. 1, pp. 87–136, 2004.
View at: Publisher Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
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 Site | Google Scholar
R. Yehuda, “Biology of posttraumatic stress disorder,” Journal of Clinical Psychiatry, vol. 62, supplement 17, pp. 41–46, 2001.
View at: Google Scholar
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 Site | Google Scholar

Copyright

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.

PDF Download Citation Order printed copies

Views

700

Downloads

1629

Citations