Skip to main content
Log in

Behavioral Depression-Related Modifications of the Properties of Glutamatergic Synapses in the Basolateral Amygdalar Nucleus in Rats

  • Published:
Neurophysiology Aims and scope

Abstract

Behavioral depression evoked by social isolation of experimental rats was accompanied by changes in the properties of glutamatergic synapses in the basolateral amygdalar nucleus, BLAN; the amplitude of field EPSP (fEPSP) decreased, long-term potentiation was intensified, while long-term depression of synaptic transmission was weakened. These modifications could be reproduced in vitro by application of 100 nM deoxycorticosterone or, partially, of 1 μM prednisolone to brain slices of intact rats, but were absent in the case of application of 100 nM dexamethasone. Observed in vivo social isolation-evoked changes in the properties of glutamatergic synapses could be prevented by subcutaneous injections of 2 mg/kg spironolactone (twice a day over 72 h of isolation). In vitro, 2 μM spironolactone eliminated modulating effects of deoxycorticosterone and inverted effects of prednisolone on the plastic properties of glutamatergic synapses. Inhibitors of transcription and ribosomal protein synthesis, doxorubicin (100 μM) and levomycetin (2 mM), respectively, prevented effects of deoxycorticosterone on synaptic transmission. The influence of the latter hormone on synaptic transmission in the BLAN was suppressed by an inhibitor of protein kinase C, polymixin B (50 μM), but significantly increased by an inhibitor of tyrosine phosphatases, sodium orthovanadate (1 mM). Suppression of synaptic transmission, which was evoked by deoxycorticosterone, was not accompanied by changes in the paired-pulse facilitation and amplitude of the NMDA component of fEPSP, while the amplitude of the AMPA component decreased. We suppose that these changes are based on intensification of synthesis of the proteins involved in endocytosis of the AMPA receptors, which results in intensification of endocytosis and a drop in the number of AMPA receptors in the postsynaptic thickenings. These changes of the fundamental properties of synaptic transmission facilitate the development of long-term potentiation of synaptic transmission, but weaken long-term depression of the transmission. The pattern of deoxycorticosterone-induced modifications of the plastic properties of glutamatergic synapses corresponds well to the main statements of the theory of metaplasticity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. I. I. Abramets, Yu. V. Kuznetsov, and I. M. Samoilovich, “Changes of properties of glutamatergic synapses in the hippocampus of rats with behavioral depression and modeling of the changes in vitro,” Neirofiziologiya/Neurophysiology, 33,No. 5, 294–303 (2001).

    Google Scholar 

  2. K. Yu. Il'yuchenok, M. A. Gilinskii, L. V. Loskutova, et al., The Amygdalar Complex: Connections, Behavior, Memory [in Russian], Nauka, Novosibirsk (1981).

    Google Scholar 

  3. L. Cahill and J. L. McGaugh, “Mechanisms of emotional arousal and lasting declarative memory,” Trends Neurosci., 21, 294–299 (1998).

    Google Scholar 

  4. M. T. Rogen, U. V. Staubli, and J. E. LeDoux, “Fear conditioning induces associative long-term potentiation in the amygdala,” Nature, 390, 604–607 (1997).

    Google Scholar 

  5. S. N. Mosalov, Clinical Application of Modern Antidepressants [in Russian], Med. Inform. Agency, Saint Petersburg (1995).

    Google Scholar 

  6. Yu. L. Nouller, Depression and Depersonalization [in Russian], Meditsina, Leningrad (1981).

    Google Scholar 

  7. P. P. Golikov, A. S. Babkova, and S. I. Potapova, “Effects of glucocorticoids on the level of transcortin-like cytoplasmic receptors,” Probl. Éndokrinol., 6, 65–68 (1979).

    Google Scholar 

  8. E. R. de Kloet, N. Y. Rots, D. M. Van Den Berg, et al., “Brain mineralocorticoid receptor function,” Ann. New York Acad. Sci., 746, 8–19 (1994).

    Google Scholar 

  9. M. Aronson, K. Fuxe, and Y. Dong, “Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization,” Proc. Natl. Acad. Sci. USA, 85, 9331–9335 (1988).

    Google Scholar 

  10. J. M. N. M. Reul and E. R. de Kloet, “Anatomical resolution of two types of corticosterone receptor sites in rat brain in vitro autoradiography and computerized image analysis,” J. Steroid Biochem. Mol. Biol., 24, 269–272 (1986).

    Google Scholar 

  11. E. R. de Kloet, “Brain corticosteroid receptor balance and homeostatic control,” Front. Neuroendocrinol., 12, 95–164 (1991).

    Google Scholar 

  12. M. J. Meaney, D. O'Donnel, V. Viau, et al., “Corticosteroid receptors in the rat brain and pituitary during development and hypothalamic-pituitary-adrenal function,” Growth Factors Hormones, 1, 163–201 (1993).

    Google Scholar 

  13. K. L. Burnstein, D. L. Bellingham, C. Jewell, et al., “Autoregulation of glucocorticoid receptor gene expression,” Steroids, 56, 52–58 (1991)

    Google Scholar 

  14. J. C. Welster and J. A. Cidlowski, “Down-regulation of the glucocorticoid receptor. A mechanism for physiological adaptation to hormones,” Ann. New York Acad. Sci., 746, 216–220 (1994).

    Google Scholar 

  15. M. Passafaro, V. Piech, and M. Sheng, “Subunit specific temporal and spatial pattern of AMPA receptor exocytosis in hippocampal neurons,” Nat. Neurosci., 4, 917–926 (2001).

    Google Scholar 

  16. W. Bai and N. L. Weigel, “Phosphorylation and steroid hormone action,” Vitamins Hormones, 51, 289–313 (1995).

    Google Scholar 

  17. K. Fukunaga and E. Miyamoto, “Role of MAP kinases in neurons,” Mol. Neurobiol., 16, 79–95 (1998).

    Google Scholar 

  18. I. I. Abramets, I. V. Komissarov, T. I. Korol', et al., “A study of the effects of nootropes on glutamatergic synaptic transmission in the rat hippocampal slices,” Arkh. Klin. Éksp. Med., 3, 13–18 (1994).

    Google Scholar 

  19. A. Arai, A. Guidotto, E. Costa, et al., “Effect of AMPA receptor modulator IDRA 21 on LTP in hippocampal slices,” NeuroReport, 7, 2211–2215 (1996).

    Google Scholar 

  20. M. Bertolino, M. Bataldi, C. Parenti, et al., “Modulation of AMPA/kainate receptors by analogues of diazoxide and cyclothiazide in thin slices of rat hippocampus,” Receptors Channels, 1, 267–278 (1993).

    Google Scholar 

  21. C. C. Huang, Y. C. Liang, and K. S. Hsu, “A role for extracellular adenosine in the time-dependent reversal of long-term potentiation by low-frequency stimulation at hippocampal CA1 synapses,” J. Neurosci., 19, 9728–9738 (1999).

    Google Scholar 

  22. S. Fujii, Y. Kuroda, K. Ito, et al., “Effects of adenosine receptors on the synaptic and EPSP-spike components of long-term potentiation and depotentiation in the guinea-pig hippocampus,” J. Physiol., 521, 451–466 (1999).

    Google Scholar 

  23. D. Yaniv and G. Richter-Levin, “LTP in rat basal amygdala induced by perirhinal cortex stimulation in vivo,” NeuroReport, 11, 525–530 (2000).

    Google Scholar 

  24. S. Maren, “Long-term potentiation in the amygdala: a mechanism for emotional learning and memory,” Trends Neurosci., 22, 561–567 (1999).

    Google Scholar 

  25. S. J. Wang and P. W. Gean, “Long-term depression of excitatory synaptic transmission in the rat amygdala,” J. Neurosci., 19, 10656–10663 (1999).

    Google Scholar 

  26. H. Wang and J. J. Wagner, “Priming-induced shift in synaptic plasticity in the rat hippocampus,” J. Neurophysiol., 82, 2024–2028 (1999).

    Google Scholar 

  27. H. Gurden J. P. Tassin, and T. M. Jay, “Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal long-term potentiation,” Neuroscience, 94, 1019–1027 (1999).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abramets, I.I., Kuznetsov, Y.V. & Samoilovich, I.M. Behavioral Depression-Related Modifications of the Properties of Glutamatergic Synapses in the Basolateral Amygdalar Nucleus in Rats. Neurophysiology 34, 273–282 (2002). https://doi.org/10.1023/A:1021215229764

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1021215229764

Navigation