Advertisement

Neuroscience and Behavioral Physiology

, Volume 47, Issue 8, pp 948–959 | Cite as

“Unpredictable Stress”: Ambiguity of Stress Reactivity in Studies of Long-Term Plasticity

  • I. V. Kudryashova
  • N. V. Gulyaeva
Article
  • 30 Downloads

Data on the influences of stress on the function of long-term synaptic plasticity are analyzed. Using longterm potentiation (LTP) as an example, stress has been shown to have both stimulatory and inhibitory influences on the effectiveness of the induction of long-term modifications, the effect depending on the nature, duration, and intensity of the stress, the observation time point, the brain structure being studied, and, thus, the involvement in the stress response of the different mechanisms underlying LTP. Stress-induced increases in glucocorticoid levels did not obligately correlate with changes in long-term plasticity, while application of corticosterone in vivo and in vitro could lead to both activation and inhibition of LTP. Existing data provide evidence that changes in LTP are determined by the ratio of mineralocorticoid and glucocorticoid receptors, activation of the latter not so much impairing the mechanisms of generation as increasing the threshold of induction of LTP, regulating the metaplasticity of synapses. The unpredictability of the effects of stress is related in particular to the involvement of other transmitter systems regulating metaplasticity whose actions depend on the animal’s individual experience in the stress reaction. The range of individual differences stimulates the ongoing search for significant factors determining the stress reactivity of longterm plasticity underlying stress resistance or susceptibility to its pathological consequences. Differences in the processing of signals arriving at neurons and their molecular mediation may constitute such a factor.

Keywords

stress stress reactivity hippocampus long-term potentiation synaptic depression synaptic metaplasticity corticosteroids glucocorticoid receptors mineralocorticoid receptors 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ahmed, T., Frey, J. U., and Korz, V., “Long-term effects of brief acute stress on cellular signaling and hippocampal LTP,” J. Neurosci., 26, 3951–3958 (2006).PubMedCrossRefGoogle Scholar
  2. Akirav, I. and Richter-Levin, G., “Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat,” J. Neurosci., 19, 10,530–10,535 (1999).Google Scholar
  3. Akirav, I. and Richter-Levin, G., “Mechanisms of amygdala modulation of hippocampal plasticity,” J. Neurosci., 22, 9912–9921 (2002).PubMedGoogle Scholar
  4. Aldenhoff, J. B., Gruol, D. L., Rivier, J., et al., “Corticotropin releasing factor decreases postburst hyperpolarizations and excites hippocampal neurons,” Science, 221, 875–877 (1983).PubMedCrossRefGoogle Scholar
  5. Aleisa, A. M., Alzoubi K. H., Gerges, N. Z., and Alkadhi, K. A., “Nicotine blocks stress-induced impairment of spatial memory and long-term potentiation of the hippocampal CA1 region,” Int. J. Neuropsychopharmacol., 9, No. 4, 417–426 (2006).PubMedCrossRefGoogle Scholar
  6. Alfarez, D. N., Wiegert, O., Joëls, M., and Krugers, H. T. “Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation,” Neuroscience, 115, No. 4, 1119–1126 (2002).PubMedCrossRefGoogle Scholar
  7. Arima-Yoshida, E., Watabe, A. M., and Manabe, T., “The mechanisms of the strong inhibitory modulation of long-term potentiation in the rat dentate gyrus,” Eur. J. Neurosci., 33, 1637–1646 (2011).PubMedCrossRefGoogle Scholar
  8. Artola, A., von Frijtag, J. C., Fermont, P. C., et al., “Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment,” Eur. J. Neurosci., 23, No. 1, 261–272 (2006).PubMedCrossRefGoogle Scholar
  9. Avital, A., Segal, M., and Richter-Levin, G., “Contrasting roles of corticosteroid receptors in hippocampal plasticity,” J. Neurosci., 26, 9130–9134 (2006).PubMedCrossRefGoogle Scholar
  10. Basta-Kaim, A., Szczesny, E., Glombik, K., et al., “Prenatal stress leads to changes in IGF-1 binding proteins network in the hippocampus and frontal cortex of adult male rat,” Neuroscience, 274, 59–68 (2014).PubMedCrossRefGoogle Scholar
  11. Blank, T., Nijholt, L., and Spiess, J., “Molecular determinants mediating effects of acute stress on hippocampus-dependent synaptic plasticity and learning,” Mol. Neurobiol., 29, 131–138 (2004).PubMedCrossRefGoogle Scholar
  12. Blank, T., Nijholt, L., Eckart, K., and Spiess, J., “Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning,” J. Neurosci., 22, 3788–3794 (2002).PubMedGoogle Scholar
  13. Bobula, B., Sowa, J., and Hess, G., “Anti-interleukin-1 antibody prevents the occurrence of repeated restraint stress-induced alterations in synaptic transmission and long-term potentiation in the rat frontal cortex,” Pharm Rep., 67, No. 1, 123–128 (2015).CrossRefGoogle Scholar
  14. Bobula, B., Wabno, J., and Hess, G., “Imipramine counteracts corticosterone-induced enhancement of glutamatergic transmission and impairment of long-term potentiation in the rat frontal cortex,” Pharm. Rep., 63, 1404–1412 (2011).CrossRefGoogle Scholar
  15. Boume, J. N. and Harris, K. M., “Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP,” Hippocampus, 21, 354–373 (2011).CrossRefGoogle Scholar
  16. Bramham, C. R., Southard, T., Ahlers S., T., and Sarvey, J. M., “Acute cold stress leading to elevated corticosterone neither enhances synaptic efficacy nor impairs LTP in the dentate gyrus of freely moving rats,” Brain Res., 789, No. 2, 245–255 (1998).PubMedCrossRefGoogle Scholar
  17. Brunson, K. L., Kramar, E., Lin, B., Chen, Y., et al., “Mechanisms of late-onset cognitive decline after early-life stress,” J. Neurosci., 25, No. 41, 9328–9338 (2005).PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cazakoff, B. N. and Howland, J. G., “Acute stress disrupts paired pulse facilitation and long-term potentiation in rat dorsal hippocampus through activation of glucocorticoid receptors,” Hippocampus, 20, 1327–1331 (2010).PubMedCrossRefGoogle Scholar
  19. Cestari, V., Rossi-Arnaud, C., Saraulli, D., and Costanzi, M., “The MAP(K) of fear: from memory consolidation to memory extinction,” Brain Res. Bull., 105, 8–16 (2014).PubMedCrossRefGoogle Scholar
  20. Chameau, P., Qin, Y., Spijker, S., et al., “Glucocorticoids specifically enhance L-type calcium current amplitude and affect calcium channel subunit expression in the mouse hippocampus,” J. Neurophysiol., 97, No. 1, 5–14 (2007).PubMedCrossRefGoogle Scholar
  21. Champagne, D. L., Bagot, R. C., van Hasselt, E., et al., “Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress,” J. Neurosci., 28, No. 23, 6037–6045 (2008).PubMedCrossRefGoogle Scholar
  22. Charil, A., Laplante, D. P., Vaillancourt, C., and King, S., “Prenatal stress and brain development,” Brain Res. Rev., 65, 56–79 (2010).PubMedCrossRefGoogle Scholar
  23. Chen, J. L., Lin, W. C., Cha J., W., So, P. T., et al.,“ Structural basis for the role of inhibition in facilitating adult brain plasticity,” Nat. Neurosci., 14, 587–594 (2011).PubMedPubMedCentralCrossRefGoogle Scholar
  24. Chen, Y., Fenoglio, K. A., Dubé, C. M., et al., “Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent,” Mol. Psychiatry, 11, No. 11, 992–1002 (2006).PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chiuccariello, L., Houle, S., Miler, L., et al., “Elevated monoamine oxidase a binding during major depressive episodes is associated with greater severity and reversed neurovegetative symptoms,” Neuropsycho pharmacology, 39, No. 4, 973–980 (2014).CrossRefGoogle Scholar
  26. Conboy, L. and Sandi, C., “Stress at learning facilitates memory formation by regulating AMPA receptor trafficking through a glucocorticoid action,” Neuropsychopharmacology, 35, 674–685 (2010).PubMedCrossRefGoogle Scholar
  27. de Kloet, E. R., Joels, M., and Holsboer, E., “Stress and the brain: from adaptation to disease,” Nat. Rev. Neurosci., 6, No. 6, 463–475 (2005).PubMedCrossRefGoogle Scholar
  28. de Kloet, E. R., Oitzl, M. S., and Jols, M., “Stress and cognition: are corticosteroids good or bad guys?” Trends Neurosci., 22, No. 10, 422–426 (1999).PubMedCrossRefGoogle Scholar
  29. Diamond, D. M., Bennett, M. C., Fleshner, M., and Rose, G. M., “Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation,” Hippocampus, 2, No. 4, 421–430 (1992).PubMedCrossRefGoogle Scholar
  30. Diamond, D. M., Park, C. R., and Woodson, J. C., “Stress generates emotional memories and retrograde amnesia by inducing an endogenous form of hippocampal LTP,” Hippocampus, 14, No. 3, 281–291 (2004).PubMedCrossRefGoogle Scholar
  31. Diamond, D. M., Park, C. R., Campbell, A. M., and Woodson, J. C., “Competitive interactions between endogenous LTD and LTP in the hippocampus underlie the storage of emotional memories and stress-induced amnesia,” Hippocampus, 15, No. 8, 1006–1025 (2005).PubMedCrossRefGoogle Scholar
  32. Dreyer, B. D., Riedel, G., and Platt, B., “The cholinergic system and hippocampal plasticity,” Behav. Brain Res., 221, 505–514 (2011).CrossRefGoogle Scholar
  33. Fa, M., Xia, L., Anunu, R., et al., “Stress modulation of hippocampal activity-spotlight on the dentate gyrus,” Neurobiol. Learn. Mem, 112, 53–60 (2014).PubMedCrossRefGoogle Scholar
  34. Fabricius, K., Wörtwein, G., and Pakkenberg, B., “The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus,” Brain Struct. Funct., 212, 403–416 (2008).PubMedPubMedCentralCrossRefGoogle Scholar
  35. Feldman, D. E., “The spike-timing dependence of plasticity,” Neuron, 75, 556–571 (2012).PubMedPubMedCentralCrossRefGoogle Scholar
  36. Finsterwald, C. and Alberini, C. M., “Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: from adaptive responses to psychopathologies,” Neurobiol. Learn. Mem, 112, 17–29 (2014).PubMedCrossRefGoogle Scholar
  37. Fontella, F. U., Vendite, D. A., Tabajara, A. S., et al., “Repeated restraint stress alters hippocampal glutamate uptake and release in the rat,” Neurochem. Res., 29, No. 9, 1703–1709 (2004).PubMedCrossRefGoogle Scholar
  38. Franklin, T. B., Linder, N., Russig, H., et al., “Influence of early stress on social abilities and serotonergic functions across generations in mice,” PLoS One, 6, e21842 (2011).PubMedPubMedCentralCrossRefGoogle Scholar
  39. Frey, S., Bergado-Rosado, J., Seindenbecher, T., et al., “Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP,” J. Neurosci., 21, 3697–3703 (2001).PubMedGoogle Scholar
  40. Fritschy, J. and Panzanelli, P., “GABAA receptors and plasticity of inhibitory neurotransmission in the central nervous system,” Eur. J. Neurosci., 39, 1845–1865 (2014).PubMedCrossRefGoogle Scholar
  41. Gadek-Michalska, A. and Bugajski, J., “Repeated handling, restraint, or chronic crowding impair the hypothalamic pituitary-adrenocortical response to acute restraint stress,” J. Physiol. Pharmacol., 54, 449–459 (2003).PubMedGoogle Scholar
  42. Gibbs, M. E., Hutchinson, D. S., and Summers, R. J., “Role of betaadrenoceptors in memory consolidation: beta3-adrenoceptors act on glucose uptake and beta2-adrenoceptors on glycogenolysis,” Neuropsycho pharmacology, 33, 2384–2397 (2008).CrossRefGoogle Scholar
  43. Godukhin, O. V., “The role of cytokines in the development of convulsive activity in the brain,” Zh. Vyssh. Nerv. Deyat., No. 5, 541–552 (2007).Google Scholar
  44. Grigor’yan, G. A. and Gulyaeva, N. V., “Stress reactivity and stress resistance in the pathogenesis of depressive disorders: the role of epigenetic mechanisms,” Zh. Vyssh. Nerv. Deyat., 65, No. 1, 19–32 (2015).Google Scholar
  45. Grigor’yan, G. A., Dygalo, N. N., Gekht, A. B., et al., “Molecular cellular mechanisms of depression. The roles of glucocorticoids, cytokines, neurotransmitters, and trophic factors in the genesis of depressive disorders,” Usp. Fiziol. Nauk, 45, No. 2, 3–19 (2014).Google Scholar
  46. Grigoryan, G., Ardi, Z., Albrecht, A., et al., “Juvenile stress alters LTP in ventral hippocampal slices: involvement of noradrenergic mechanisms,” Behav. Brain Res., 278, 559–562 (2015).PubMedCrossRefGoogle Scholar
  47. Groc, L., Choquet, D., and Chaouloff, E., “The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation,” Nat. Neurosci., 11, 868–870 (2008).PubMedCrossRefGoogle Scholar
  48. Groeneweg, E. L., Karst, H., de Kloet, E. R., and Joels, M., “Rapid nongenomic effects of corticosteroids and their role in the central stress response,” J. Endocrinol., 209, 153–167 (2011).PubMedCrossRefGoogle Scholar
  49. Grunewald, M., Johnson, S., Lu, D., et al., “Mechanistic role for a novel glucocorticoid-KLF11 (TIEG2) protein pathway in stress-induced monoamine oxidase A expression,” J. Biol. Chem., 287, No. 29, 24195–24206 (2012).PubMedPubMedCentralCrossRefGoogle Scholar
  50. Gulyaeva, N. V., “Fundamental and translational aspects of the stress reactivity of the ventral hippocampus: functional biochemical mechanisms of changes in neuroplasticity,” Neirokhimiya, No. 2, 101–111 (2015).Google Scholar
  51. Hayama, T., Noguchi, J., Watanabe, S., et al., “GABA promotes the competitive selection of dendritic spins by controlling local Ca2+ signaling,” Nat. Neurosci., 16, No. 10, 1409–1416 (2013).PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hewitt, S. A., Wamsteeker, J. I., Kurz E.,U., and Bains, J. S., “Altered chloride homeostasis removes synaptic inhibitory constraint of the stress axis,” Nat. Neurosci., 12, 438–443 (2009).PubMedCrossRefGoogle Scholar
  53. Hiraide, S., Saito, Y., Matsumoto, M., et al., “Possible modulation, of the amygdala on metaplasticity deficits in the hippocampal CA1 field in early postnatally stressed rats,” J. Pharmacol. Sci., 119, 64–72 (2012).PubMedCrossRefGoogle Scholar
  54. Hirata, R., Matsumoto, M., Judo, C., et al., “Possible relationship between the stress-induced synaptic response and metaplasticity in the hippocampal CA1 field of freely moving rats,” Synapse, 63, No. 7, 549–556 (2009).PubMedCrossRefGoogle Scholar
  55. Holm, M. M., Nieto-Gonzalez, I. L., Vardya, I., et al., “Hippocampal GABA - ergic dysfunction in a rat chronic mild stress model of depression,” Hippocampus, 21, No. 4, 422–433 (2011).PubMedCrossRefGoogle Scholar
  56. Holmes, A. and Wellman, C. L., “Stress-induced prefrontal reorganization and executive dysfunction in rodents,” Neurosci. Biobehav. Rev., 33, 773–783 (2009).PubMedCrossRefGoogle Scholar
  57. Howland, I. G. and Wang, Y. T., “Synaptic plasticity in learning and memory: stress effects in the hippocampus,” Prog. Brain Res., 169, 145–158 (2008).PubMedCrossRefGoogle Scholar
  58. Hu, W., Zhang, M., Czeh, B., et al., “Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin-expressing neuronal network,” Neuropsychopharmacology, 35, 1693–1707 (2010).PubMedPubMedCentralGoogle Scholar
  59. Huang, C. C., Yang, C. H., and Hsu, K. S., “Do stress and long-term potentiation share the same molecular mechanisms?” Mol. Neurobiol., 32, No. 3, 223–235 (2005).PubMedCrossRefGoogle Scholar
  60. Inoue, W. and Bains, J. S., “Beyond inhibition: GABA synapses tune the neuroendocrine stress axis,” Bioessays, 36, 561–569 (2014).PubMedCrossRefGoogle Scholar
  61. Inoue, W., Baimoukhametova D. V., Fuzesi, T., et al., “Noradrenaline is a stress-associated metaplastic signal at GABA synapses,” Nat. Neurosci., 16, No. 5, 605–612 (2013).PubMedPubMedCentralCrossRefGoogle Scholar
  62. Ishikawa, S., Saito, Y., Yanagawa, Y., et al., “Early postnatal stress alters extracellular signal-regulated kinase signaling in the corticolimbic system modulating emotional circuitry in adult rats,” Eur. J. Neurosci., 35, No. 1, 135–145 (2012).PubMedCrossRefGoogle Scholar
  63. Jin, Y., Kanno, T., and Nishizaki, T., “Acute restraint stress impairs induction of long-term potentiation by activating GSK3β,” Neurochem. Res., 40, No. 1, 36–40 (2015).PubMedCrossRefGoogle Scholar
  64. Joels, M. and Krugers, H. T., “LTP after Stress: Up or Down?” Neural Plast., 2007, 93202 (2007).Google Scholar
  65. Joels, M., “Corticosteroid effects in the brain: U-shape it,” Trends Pharmacol. Sci., 27, 5, 244–250 (2006).PubMedCrossRefGoogle Scholar
  66. Joels, M., “Stress, the hippocampus, and epilepsy,” Epilepsia, 50, 586–597 (2009).PubMedCrossRefGoogle Scholar
  67. Joels, M., Karst, H., DeRijk, R., and de Kloet, E. R., “The coming out of the brain mineralocorticoid receptor,” Trends Neurosci., 31, No. 1, 1–7 (2008).PubMedCrossRefGoogle Scholar
  68. Joels, M., Krugers, H. J., Lucassen, P. I., and Karst, H., “Corticosteroid effects on cellular physiology of limbic cells,” Brain Res., 293, 91–100 (2009).CrossRefGoogle Scholar
  69. Joels, M., Velzing, E., Nair, W., et al., “Acute stress increases calcium current amplitude in rat hippocampus: temporal changes in physiology and gene expression,” Eur. J. Neurosci., 18, 1315–1324 (2003).PubMedCrossRefGoogle Scholar
  70. Kallarackal, A. J., Kvarta, M. D., Cammarata, E., et al., “Chronic stress induces a selective decrease in AMPA receptor-mediated synaptic excitation at hippocampal temporoammonic-CA1 synapses,” J. Neurosci., 33, No. 40, 15,669–15,674 (2013).Google Scholar
  71. Kamal, A., Ramakers, G. M., Altinbilek, B., and Kas, M. J., “Social isolation stress reduces hippocampal long-term potentiation: effect of animal strain and involvement of glucocorticoid receptors,” Neuroscience, 256, 262–270 (2014).PubMedCrossRefGoogle Scholar
  72. Karst, H., Berger, S., Erdmann, G., et al., “Metaplasticity of amygdalar responses to the stress hormone corticosterone,” Proc. Natl. Acad. Sci. USA, 107, 14449–14454 (2010).PubMedPubMedCentralCrossRefGoogle Scholar
  73. Karst, H., Berger, S., Turiault, M., et al., “Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone,” Proc. Natl. Acad. Sci. USA, 102, No. 52, 19204–19207 (2005).PubMedPubMedCentralCrossRefGoogle Scholar
  74. Karst, H., Wadman, W. J., and Joëls, M., “Corticosteroid receptor-dependent modulation of calcium currents in rat hippocampal CA1 neurons,” Brain Res., 649, No. 1–2, 234–242 (1994).PubMedCrossRefGoogle Scholar
  75. Kavushansky, A., Vouimba, R. M., Cohen, H., and Richter-Levin, G., “Acti vity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress,” Hippocampus, 16, No. 1, 35–42 (2006).PubMedCrossRefGoogle Scholar
  76. Kim Ji, Song E.,Y. , and Kosten, T. A.,“ Stress effects in the hippocampus: synaptic plasticity and memory,” Stress, 9, 1–11 (2006).CrossRefGoogle Scholar
  77. Kim, J. J., Koo, J. W., Lee, H. J., and Han, J. S., “Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory,” J. Neurosci., 25, No. 6, 1532–1539 (2005) .PubMedCrossRefGoogle Scholar
  78. Kleschevnikov, A. M., Belichenko, P. V., Villar, A. J., et al., “Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome,” J. Neurosci., 24, 8153–8160 (2004).PubMedCrossRefGoogle Scholar
  79. Kleshchevnikov, A. M. and Voronin, L. L., “Repeated induction of longterm potentiation after its saturation in living hippocampal slices from rats,” Dokl. Akad. Nauk, 340, No. 5, 694–696 (1995).PubMedGoogle Scholar
  80. Korz, V. and Frey, J. U., “Stress-related modulation of hippocampal longterm potentiation in rats: involvement of adrenal steroid receptors,” J. Neurosci., 23, No. 19, 7281–7287 (2003).PubMedGoogle Scholar
  81. Krugers H. J., Alfarez, D. N., Karst, H., et al., “Corticosterone shifts different forms of synaptic potentiation in opposite directions,” Hippocampus, 15, No. 6, 697–703 (2005).PubMedCrossRefGoogle Scholar
  82. Kudryashova, I. V., “Plasticity of inhibitory synapses as a factor in longterm modifications,” Neirokhimiya, 32, No. 3, 181–191 (2015).Google Scholar
  83. Lanfumey, L., Mongeau, R., Cohen-Salmon, C., and Hamon, M., “Corticos teroid-serotonin interactions in the neurobiological mechanisms of stress-related disorders,” Neurosci. Biobehav. Rev., 32, 1174–1184 (2008).PubMedCrossRefGoogle Scholar
  84. Lapiz, M. D., Fulford, A., Muchimapura, S., et al., “Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission ,” Neurosci. Behav. Physiol., 33, No. 1, 13–29 (2003).Google Scholar
  85. Lee, E. J., Son, G. H., Chung, S., et al., “Impairment of fear memory consolidation in maternally stressed male mouse offspring: Evidence for nongenomic glucocorticoid action on the amygdala,” J. Neurosci., 31, No. 19, 7131–7140 (2011).PubMedCrossRefGoogle Scholar
  86. Lee, S. Y., Hwang, Y. K., Yun, H. S., and Han, J. S., “Decreased levels of nuclear glucocorticoid receptor protein in the hippocampus of aged Long-Evans rats with cognitive impairment,” Brain Res., 1478, 48–54 (2012).PubMedCrossRefGoogle Scholar
  87. Lim, C. S., Kim Yi, Hwang, Y. K., et al., “Decreased interactions in protein kinase A-Glucocorticoid receptor signaling in the hippocampus after selective removal of the basal forebrain cholinergic input,” Hippocampus, 22, 455–465 (2012).PubMedCrossRefGoogle Scholar
  88. Liu, M., Li, J., Dai, P., et al., “Microglia activation regulates GluR1 phosphorylation in chronic unpredictable stress-induced cognitive dysfunction,” Stress, 18, No. 1, 96–106 (2015).PubMedCrossRefGoogle Scholar
  89. Lopes Aguiar, C., Romcy-Pereira, R. N., Escorsim Szawka, R., et al., “Mus carinic acetylcholine neurotransmission enhances the latephase of long-term potentiation in the hippocampal-prefrontal cortex pathway of rats in vivo: a possible involvement of monoaminergic systems,” Neuroscience, 153, No. 4, 1309–1319 (2008).PubMedCrossRefGoogle Scholar
  90. Lupien, S. J., McEwen, B. S., Gunnar, M. R., and Heim, C., “Effects of stress throughout the lifespan on the brain, behavior and cognition,” Nat. Rev. Neurosci., 10, 434–445 (2009).PubMedCrossRefGoogle Scholar
  91. Lussier, A. L., Romay-Tallon, R., Caruncho, H. J., and Kalynchuk, L. E., “Altered GABAergic and glutamatergic activity within the rat hippocampus and amygdala in rats subjected to repeated corticosterone administration but not restraint stress,” Neuroscience, 231, 38–48 (2013).PubMedCrossRefGoogle Scholar
  92. Maccari, S., Krugers, H. J., Morley-Fletcher, S., et al., “The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations,” J. Neuroendocrinol., 26, 707–723 (2014).PubMedCrossRefGoogle Scholar
  93. MacDougall, M. J. and Howland, J.G., “Acute stress and hippocampal output: exploring dorsal CA1 and subicular synaptic plasticity simultaneously in anesthetized rats,” Physiol. Rep., 1, No. 2, e00035 (2013).PubMedPubMedCentralCrossRefGoogle Scholar
  94. Maggio, N. and Segal, M., “Cellular basis of a rapid effect of mineralocorticosteroid receptors activation on LTP in ventral hippocampal slices,” Hippocampus, 22, No. 2, 267–275 (2012).PubMedCrossRefGoogle Scholar
  95. Maggio, N. and Segal, M., “Differential corticosteroid modulation of inhibitory synaptic currents in the dorsal and ventral hippocampus,” J. Neurosci., 29, No. 9, 2857–2866 (2009a).PubMedCrossRefGoogle Scholar
  96. Maggio, N. and Segal, M., “Differential modulation of long-term depression by acute stress in the rat dorsal and ventral hippocampus,” J. Neurosci., 29, No. 27, 8633–8638 (2009b).PubMedCrossRefGoogle Scholar
  97. Maggio, N. and Segal, M., “Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus,” J. Neurosci., 27, No. 21, 5757–5765 (2007).PubMedCrossRefGoogle Scholar
  98. Maguire, J. and Mody, I., “Steroid hormone fluctuations and GABA(A)R plasticity,” Psychoneuroendocrinology, 34, S84–S90 (2009).PubMedPubMedCentralCrossRefGoogle Scholar
  99. Marmigere, E., Givalois, L., Rage, E., et al., “Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats,” Hippocampus, 13, 646–655 (2003).PubMedCrossRefGoogle Scholar
  100. Maroun, M., “Stress reverses plasticity in the pathway projecting from the ventromedial prefrontal cortex to the basolateral amygdala,” Eur. J. Neurosci., 24, No. 10, 2917–2922 (2006).PubMedCrossRefGoogle Scholar
  101. Martin, S., Henley, J. M., Holman, D., et al., “Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity,” PLoS One, 4, No. 3, e4714 (2009).PubMedPubMedCentralCrossRefGoogle Scholar
  102. Matsumoto, K., Puia, G., Dong, E., and Pinna, G., “GABA(A) receptor neu ro transmission dysfunction in a mouse model of social isolation-induced stress: possible insights into a non-serotonergic mechanism of action of SSRIs in mood and anxiety disorders,” Stress, 10, 3–12 (2007).PubMedCrossRefGoogle Scholar
  103. Matsumoto, M., Togashi, H., Ohashi, S., et al., “Serotonergic modulation of psychological stress-induced alteration in synaptic plasticity in the rat hippocampal CA1 field,” Brain Res., 1022, 221–225 (2004).PubMedCrossRefGoogle Scholar
  104. McEwen, B. S., “Physiology and neurobiology of stress and adaptation: central role of the brain,” Physiol. Rev., 87, 873–904 (2007).PubMedCrossRefGoogle Scholar
  105. McGaugh, J. L., “Making lasting memories: remembering the significant,” Proc. Natl. Acad. Sci. USA, 110, No. 2, 10402–10407 (2013).PubMedPubMedCentralCrossRefGoogle Scholar
  106. McReynolds, J. R., Donowho, K., Abdi, A., et al., “Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions,” Neurobiol. Learn. Mem, 93, 312–321 (2010).PubMedCrossRefGoogle Scholar
  107. Mesquita, A. R., Pêgo, J. M., Summavielle, T., et al., “Neurodevelopment milestone abnormalities in rats exposed to stress in early life,” Neuroscience, 147, 1022–1033 (2007).PubMedCrossRefGoogle Scholar
  108. Mora, E., Segovia, G., Del Arco, A., et al., “Stress, neurotransmitters, corticosterone and body-brain integration,” Brain Res., 1476, 71–85 (2012).PubMedCrossRefGoogle Scholar
  109. Musazzi, L., Racagni, G., and Popoli, M., “Stress, glucocorticoids and glutamate release: Effects of antidepressant drugs,” Neurochem. Int., 59, 138–149 (2011).PubMedCrossRefGoogle Scholar
  110. Nikzad, S., Vafaei, A. A., Rashidy-Pour, A., and Haghighi, S. “Systemic and intrahippocampal administrations of the glucocorticoid receptor antagonist RU38486 impairs fear memory reconsolidation in rats,” Stress, 14, 459–464 (2011).PubMedCrossRefGoogle Scholar
  111. Olijslagers, J. E, de Kloet, E. R., Elgersma, Y., et al., “Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors,” Eur. J. Neurosci., 27, No. 10, 2542–2550 (2008).PubMedCrossRefGoogle Scholar
  112. Oomen, C. A., Soeters, H., Audureau, N., et al., “Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood,” J. Neurosci., 30, 6635–6645 (2010).PubMedCrossRefGoogle Scholar
  113. Paille, V., Fino, E., Du, K., et al., “GABAergic circuits control spike-timing-dependent plasticity,” J. Neurosci., 33, No. 22, 9353–9363 (2013).PubMedCrossRefGoogle Scholar
  114. Park, H. J., Lee, S., Jung, J. W, et al., “Glucocorticoid- and long-term stress-induced aberrant synaptic plasticity are mediated by activation of the glucocorticoid receptor ,” Arch Pharm. Res., 38, No. 6, 1204–1212 (2015).PubMedCrossRefGoogle Scholar
  115. Pavlides, C., Nivon, L. G., and McEwen, B. S., “Effects of chronic stress on hippocampal long-term potentiation,” Hippocampus, 12, 2, 245–257 (2002).PubMedCrossRefGoogle Scholar
  116. Polman, J. A., de Kloet, E. R., and Datson, N. A., “Two populations of glucocorticoid receptor-binding sites in the male rat hippocampal genome,” Endocrinology, 154, 1832–1844 (2013).PubMedCrossRefGoogle Scholar
  117. Popoli, M., Yan, Z., McEwen, B. S., and Sanacora, G., “The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission,” Nat. Rev. Neurosci., 13, 22–37 (2011).PubMedPubMedCentralCrossRefGoogle Scholar
  118. Prager, E. M., Brielmaier, J., Bergstrom, H. C., et al., “Localization of mineralocorticoid receptors at mammalian synapses,” PLoS One, 5, No. 12, e14344 (2010).PubMedPubMedCentralCrossRefGoogle Scholar
  119. Qin, X., Liu, Y., Zhu, M., and Yang, Z., “The possible relationship between expressions of TRP C3/5 channels and cognitive changes in rat model of chronic unpredictable stress,” Behav. Brain Res., 290, 180–186 (2015).PubMedCrossRefGoogle Scholar
  120. Radahmadi, M., Hosseini, N., and Nasimi, A., “Effect of chronic stress on short and long-term plasticity in dentate gyrus; study of recovery and adaptation,” Neuroscience, 280, 121–129 (2014).PubMedCrossRefGoogle Scholar
  121. Radley, J. J., Rocher, A. B., Janssen, W. G., et al., “Reversibility of apical dendritic retraction in the rat media] prefrontal cortex following repeated stress,” Exp. Neurol., 196, 199–203 (2005).Google Scholar
  122. Rey, M., Carlier, E., Talmi, M., and Soumireu-Mourat, B., “Corticosterone effects on long-term potentiation in mouse hippocampal slices,” Neuroendocrinology, 60, 36–41 (1994).PubMedCrossRefGoogle Scholar
  123. Richter-Levin, G. and Maroun, M., “Stress and amygdala suppression of metaplasticity in the medial prefrontal cortex,” Cereb. Cortex, 20, No. 10, 2433–2441 (2010).PubMedCrossRefGoogle Scholar
  124. Richter-Levin, G., “The amygdala, the hippocampus, and emotional modulation of memory,” Neuroscientist, 10, No. 1, 31–39 (2004).PubMedCrossRefGoogle Scholar
  125. Roozendaal, B., “Systems mediating acute glucocorticoid effects on memory consolidation and retrieval,” Prog. Neuropsychopharmacol. Biol. Psychiatry, 27, No. 8, 1213–1223 (2003).PubMedCrossRefGoogle Scholar
  126. Roozendaal, B., McEwen, B. S., and Chattarji, S., “Stress, memory and the amygdala,” Nat. Rev. Neurosci., 10, 423–433 (2009).PubMedCrossRefGoogle Scholar
  127. Sachs, B. D., Ni, J. R., and Caron, M. G., “Sex differences in response to chronic mild stress and congenital serotonin deficiency,” Psychoneuro endocrinology, 40, 123–129 (2014).CrossRefGoogle Scholar
  128. Sarkar, J., Wakefield, S., Mackenzie, G., et al., “Neurosteroidogenesis is required for the physiological response to stress: role of neurosteroid-sensitive GABAA receptors,” J. Neurosci., 31, 18,198–18,210 (2011).Google Scholar
  129. Schayek, R. and Maroun, M., “Differences in stress-induced changes in extinction and prefrontal plasticity in postweanling and adult animals,” Biol. Psychiatry, 78, No. 3, 159–166 (2015).PubMedCrossRefGoogle Scholar
  130. Schmidt, M. V., Abraham, W. C., Maroun, M., et al., “Stress-induced metaplasticity: from synapses to behavior,” Neuroscience, 250, 112–120 (2013).PubMedCrossRefGoogle Scholar
  131. Segal, M., Richter-Levin, G., and Maggio, N., “Stress-induced dynamic routing of hippocampal connectivity: a hypothesis,” Hippocampus, 20, 1332–1338 (2010).PubMedCrossRefGoogle Scholar
  132. Serra, M., Pisu M. G., Mostallino M. C., et al., “Changes in neuroactive steroid content during social isolation stress modulate GABAA receptor plasticity and function,” Brain Res. Rev., 57, 520–530 (2008).PubMedCrossRefGoogle Scholar
  133. Sharvit, A., Segal, M., Kehat, O., et al., “Differential modulation of synaptic plasticity and local circuit activity in the dentate gyrus and CA1 regions of the rat hippocampus by corticosterone,” Stress, 18, No. 3, 319–327 (2015).PubMedCrossRefGoogle Scholar
  134. Shen, H., Sabaliauskas, N., Sherpa, A., et al., “A critical role for alpha-4betadelta GABAA receptors in shaping learning deficits at puberty in mice ,” Science, 327, No. 5972, 1515–1518 (2010).PubMedPubMedCentralCrossRefGoogle Scholar
  135. Skrebitskii V. G. and Shtark, M. B. , “Fundamental basics of nervous system plasticity,” Vestn. Ross. Akad. Med. Nauk., No. 9, 39–44 (2012).Google Scholar
  136. Slotkin, T. A., Kreider, M. L., Tate, C. A., and Seidler, E. J., “Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems,” Neuropsycho pharmacology, 31, 904–911 (2006).CrossRefGoogle Scholar
  137. Sousa, N., Cerqueira, J. J., and Almeida, O. F., “Corticosteroid receptors and neuroplasticity,” Brain Res. Rev., 57, No. 2, 561–570 (2008).PubMedCrossRefGoogle Scholar
  138. Sowa, J., Bobula, B., Glombik, K., et al., “Prenatal stress enhances excitatory synaptic transmission and impairs long-term potentiation in the frontal cortex of adult offspring rats,” PLoS One, 10, No. 3, e0119407 (2015).PubMedPubMedCentralCrossRefGoogle Scholar
  139. Spyrka, J. and Hess, G., “Repeated restraint-induced modulation of longterm potentiation in the dentate gyrus of the mouse,” Brain Res., 1320, 28–33 (2010).PubMedCrossRefGoogle Scholar
  140. Spyrka, J., Danielewicz, J., and Hess, G., “Brief neck restraint stress enhances long-term potentiation and suppresses long-term depression in the dentate gyrus of the mouse,” Brain Res. Bull., 85, 363–367 (2011).PubMedCrossRefGoogle Scholar
  141. Tsoory, M. M., Vouimba, R. M., Akirav, I., et al., “Amygdala modulation of memory-related processes in the hippocampus: potential relevance to PTSD,” Prog. Brain Res., 167, 35–51 (2008).PubMedCrossRefGoogle Scholar
  142. Venzala, E., Garcia-Garcia, A. L., Elizalde, N., and Tordera, R. M., “Social vs. environmental stress models of depression from a behavioural and neurochemical approach,” Eur. Neuropsychopharmacol., 23, No. 7, 697–708 (2013).PubMedCrossRefGoogle Scholar
  143. Verkuyl, J. M., Karst, H., and Joas, M., “GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress,” Eur. J. Neurosci., 21, 113–121 (2005).PubMedCrossRefGoogle Scholar
  144. Viviani, B., Boraso, M., Valero, M., et al., “Early maternal deprivation immunologically primes hippocampal synapses by redistributing interleukin-1 receptor type I in a sex dependent manner,” Brain Behav. Immun., 35, 135–143 (2014).PubMedCrossRefGoogle Scholar
  145. Voronin, L., Byzov, A., Kleschevnikov, A., et al., “Neurophysiological analysis of long-term potentiation in mammalian brain,” Behav. Brain Res., 66, No. 1–2, 45–52 (1995).PubMedCrossRefGoogle Scholar
  146. Vouimba, R. M. and Richter-Levin, G., “Physiological dissociation in hippocampal subregions in response to amygdala stimulation,” Cereb. Cortex, 15, 1815–1821 (2005).PubMedCrossRefGoogle Scholar
  147. Vouimba, R. M., Yaniv, D., and Richter-Levin, G., “Glucocorticoid receptors and beta-adrenoceptors in basolateral amygdala modulate synaptic plasticity in hippocampal dentate gyrus, but not in area CA1,” Neuropharmacology, 52, 244–252 (2007).PubMedCrossRefGoogle Scholar
  148. Vouimba, R. M., Yaniv, D., Diamond, D., and Richter-Levin, G., “Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats,” Eur. J. Neurosci., 19, 1887–1894 (2004).PubMedCrossRefGoogle Scholar
  149. Wang, X. D., Su, Y. A., Wagner, K. V., et al., “Nectin-3 links CRHR1 signaling to stress-induced memory deficits and spine loss,” Nat. Neurosci., 16, No. 6, 706–713 (2013).PubMedCrossRefGoogle Scholar
  150. Wiegert, O., Joëls, M., and Krugers, H. J., “Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus,” Learn. Mem., 13, No. 2, 110–113 (2006).PubMedCrossRefGoogle Scholar
  151. Wiegert, O., Pu, Z., Shor, S., et al., “Glucocorticoid receptor activation selectively hampers N-methyl-D-aspartate receptor dependent hippocampal synaptic plasticity in vitro,” Neuroscience, 135, 403–411 (2005).PubMedCrossRefGoogle Scholar
  152. Wong, D. L., Tai, T. C., Wong-Faull, D. C., et al., “Epinephrine: a shortand long-term regulator of stress and development of illness: a potential new role for epinephrine in stress,” Cell. Mol. Neurobiol., 32, No. 5, 737–748 (2012).PubMedCrossRefGoogle Scholar
  153. Woodin, M. A., Ganguly, K., and Poo, M., “Coincident pre-and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl-transporter activity,” Neuron, 39, 807–820 (2003).PubMedCrossRefGoogle Scholar
  154. Yamada, K., McEwen, B. S., and Pavlides, C., “Site and time dependent effects of acute stress on hippocampal long-term potentiation in freely behaving rats,” Exp. Brain Res., 152, No. 1, 52–59 (2003).PubMedCrossRefGoogle Scholar
  155. Yang, C.-H., Huang, C.-Ch., and Hsu, K.-S., “Behavioral stress modifies hippocampal synaptic plasticity through corticosterone-induced sustained extracellular signal-regulated kinase/mitogen-activated protein kinase activation,” J. Neurosci., 24, No. 49, 11029–11034 (2004).PubMedCrossRefGoogle Scholar
  156. Yang, E. C. and Liang, K. C., “Interactions of the dorsal hippocampus, medial prefrontal cortex and nucleus accumbens in formation of fear memory: difference in inhibitory avoidance learning and contextual fear conditioning,” Neurobiol. Learn. Mem., 112, 186–194 (2014).PubMedCrossRefGoogle Scholar
  157. Yang, P.-C., Yang, C.-H., Huang, C.-C., and Hsu, K.-S., “Phosphatidylinositol 3-kinase activation is required for stress protocol-induced modification of hippocampal synaptic plasticity,” J. Biol. Chem., 283, 2631–2643 (2008).PubMedCrossRefGoogle Scholar
  158. Yuen, E. Y., Liu, W., Karatsoreos, L. N., et al., “Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory,” Mol. Psychiatry, 16, No. 2, 156–170 (2011).PubMedCrossRefGoogle Scholar
  159. Zheng, C. and Zhang, T., “Synaptic plasticity-related neural oscillations on hippocampus-prefrontal cortex pathway in depression,” Neuro science, 292, 170–180 (2015).Google Scholar
  160. Zheng, G., Zhang, X., Chen, Y., et al., “Evidence for a role of GABAA receptor in the acute restraint stress-induced enhancement of spatial memory,” Brain Res., 1181, 61–73 (2007).PubMedCrossRefGoogle Scholar
  161. Zhu, M. Y., Wang, W. P., Huang, J., et al., “Repeated immobilization stress alters rat hippocampal and prefrontal cortical morphology in parallel with endogenous agmatine and arginine decarboxylase levels,” Neurochem. Int., 53, 346–354 (2008).PubMedPubMedCentralCrossRefGoogle Scholar
  162. Zitman, F. M., Lucas, M., Trinks, S., et al., “Dentate gyrus local circuit is implicated in learning under stress-a role for neurofascin,” Mol. Neurobiol., 53, No. 2, 842–850 (2016).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of SciencesMoscowRussia

Personalised recommendations