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Electrophysiological and morpho-histochemical study of action of adrenalectomy on hippocampal neurons

  • Comparative and Ontogenic Physiology
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Abstract

Chronic insufficiency of adrenal hormones is a pathology leading to brain dysfunction. By electrophysiological approach there were studied mechanisms of adaptation of neural networks to chronic hormonal deprivation by extracellular recording of the single spike activity of hippocampal neurons (HN), which was caused by high-frequency stimulation of the entorhinal cortex (EC) in rats with unilateral removal of adrenal (adrenalectomy—AE). The balance of excitatory and inhibitory responses recorded in intact rat HN underwent characteristic changes in dynamics of development of neurodegeneration: the inhibitory responses dominating in norm were decreased in all AE terms (from 42% to 25% by 18 weeks). On the contrary, the minimal percentage of excitatory responses in norm was sharply increased at 25–27 days after AE (from 17% to 60%), by indicating a possible increase in cholinergic neurotransmission. The high level of the mean frequency of peristimulus spiking was recorded from the 25–27th day to the 18th week after AE, which indicates the presence of the high level of glutamate or the expressed activation of NMDA receptors. On the whole, the ratio of the excitatory/inhibitory HN responses suggests discrepancy of neural activity in EC HN chains under the AE conditions. Histochemical analysis has shown an increased sensitivity to AE in the CA1 area neurons. After disruption of neuronal structure by the 5th day of AE, 25–27 days after AE, proliferation of cellular elements was observed in the CA1 area, due which the complete filling of the “devastated” areas of hippocampus and a sharp enhancement of phosphatase activity occurred by 8-10 weeks in neuronal nuclei of the dentate gyrus. By 18 weeks after AE, most neurons in the CA1 area were subjected to chromatolysis with a fall of phosphatase activity. The presented make certain contribution to understanding of mechanisms of control of cognitive function and brain plasticity with interconnection with hormonal factors.

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References

  1. Greiner, M., Cardenas, S., Parra, C., Bravo, J., Avalos, A.M., Paredes, A., Lara, H.E., and Fiedler, J.L., Adrenalectomy Regulates Apoptotic-Associated Genes in Rat Hippocampus, Endocrine., 2001, vol. 15, pp. 323–333.

    Article  PubMed  CAS  Google Scholar 

  2. Spanswick, S.C. and Sutherland, R.J., Object/Context-Specific Memory Deficits Associated with Loss of Hippocampal Granule Cells after Adrenalectomy in Rats, Learn. Mem., 2010, vol. 17, no. 5, pp. 241–245.

    Article  PubMed  CAS  Google Scholar 

  3. Hajisoltani, R., Rashidy-Pour, A., Vafaei, A.A., Ghaderdoost, B., Bandegi, A.R., and Motamedi, F., The Glucocorticoid System is Required for the Voluntary Exercise-Induced Enhancement of Learning and Memory in Rats, Behav. Brain Res., 2011, vol. 219, no. 1, pp. 75–81.

    Article  PubMed  CAS  Google Scholar 

  4. Nichols, N.R., Agolley, D., Zieba, M., and Bye, N., Glucocorticoid Regulation of Glial Responses during Hippocampal Neurodegeneration and Regeneration, Brain Res. Rev., 2005, vol. 48, no. 2, pp. 287–301.

    Article  PubMed  CAS  Google Scholar 

  5. Bravo, J.A., Parra, C.S., Arancibia, S., Andrés, S., Morales, P., Herrera-Marschitz, M., Herrera, L., Cameron, H.A., Tanapat, P., and Gould, E., Adrenal Steroids and N-methyl-D-aspartate Receptor Activation Regulate Neurogenesis in the Dentate Gyrus of Adult Rats through a Common Pathway, Neurosci., 1989, vol. 82, no. 2, pp. 349–354.

    Google Scholar 

  6. Schenk, G.J., Engels, B., Zhang, Y.P., Fitzsimons, C.P., Schouten, T., Kruidering, M., de Kloet, E.R., and Vreugdenhil, E., A Potential Role for Calcium/Calmodulin-Dependent Protein Kinase-Related Peptide in Neuronal Apoptosis: in vivo and in vitro Evidence, Eur. J. Neurosci., 2007, vol. 26, no. 12, pp. 3411–3420.

    Article  PubMed  Google Scholar 

  7. Orlov, A.I., Prikladnaya statistika (Applied Statistics), Ekzamen, Moscow, 2004.

    Google Scholar 

  8. Meliksetyan, I.B., Detection of Activity of Ca2+-Dependent Acid Phosphotase in Cellular Structures of Rat Brain, Morfologiya (St. Petersburg), 2007, vol. 131, no. 2, pp. 77–80.

    CAS  Google Scholar 

  9. Rudy, J.W., The Neurobiology of Learning and Memory, Sinauer Associates Inc., Massachusetts, 2008.

    Google Scholar 

  10. Rey, M., Carlier, E., and Soumireu-Mourat, B., Effects of Corticosterone on Hippocampal Slice Electrophysiology in Normal and Adrenalectomized BALB/c Mice, Neuroendocrinol., 1987, vol. 46, no. 5, pp. 424–429.

    Article  CAS  Google Scholar 

  11. Mizoguchi, K., Shoji, H., Ikeda, R., Tanaka, Y., Maruyama, W., and Tabira, T., Suppression of Glucocorticoid Secretion Enhances Cholinergic Transmission in Rat Hippocampus, Brain Res. Bull., 2008, vol. 76, no. 6, pp. 612–615.

    Article  PubMed  CAS  Google Scholar 

  12. Chao, H.M., Yun, L.M.A., McEwen, B.S., and Sakai, R.R., Regulation of Glucocorticoid Receptor and Mineralocorticoid Receptor Messenger Ribonucleic Acids by Selective Agonists in the Rat Hippocampus, Endocrinol., 1998, vol. 39, no. 4, pp. 1810–1814.

    Article  Google Scholar 

  13. Komuro, H. and Rakic, P., Modulation of Neuronal Migration by NMDA Receptors, Science, 1993, vol. 260, pp. 95–97.

    Article  PubMed  CAS  Google Scholar 

  14. Tsunashima, K., Schwarzer, C., Kirchmair, E., Sieghart, W., and Sperk, G., GABA(A) Receptor Subunits in the Rat Hippocampus III: Altered Messenger RNA Expression in Kainic Acid-Induced Epilepsy, Neurosci., 1997, vol. 80, no. 4, pp. 1019–1032.

    Article  CAS  Google Scholar 

  15. Earnheart, J.C., Schweizer, C., Crestani, F., Iwasato, T., Itohara, S., Mohler, H., and Lüscher, B., GABAergic Control of Adult Hippocampal Neurogenesis in Relation to Behavior Indicative of Trait Anxiety and Depression States, J. Neurosci., 2007, vol. 27, no. 14, pp. 3845–3854.

    Article  PubMed  CAS  Google Scholar 

  16. Karst, H. and Joëls, M., Calcium Currents in Rat Dentate Granule Cells Are Altered after Adrenalectomy, Eur. J. Neurosci., 2001, vol. 14, no. 3, pp. 503–512.

    Article  PubMed  CAS  Google Scholar 

  17. Dijkmans, T.F. and van Hooijdonk, L.W., The Doublecortin Gene Family and Disorders of Neuronal Structure, Cent. Nerv. Syst. Agents Med. Chem., 2010, vol. 10, no. 1, pp. 32–46.

    Article  PubMed  CAS  Google Scholar 

  18. Pedotti, P., Hoen, P.A., Vreugdenhil, E., Schenk, G.J., Vossen, R.H., Ariyurek, Y., de Hollander, M., Kuiper, R., van Ommen, G.J., den Dunnen, J.T., Boer, J.M., and de Menezes, R.X., Can Subtle Changes in Gene Expression be Consistently Determined with Different Microarray Platforms?, BMC Genomics, 2008, vol. 9, no. 124, pp. 164–169.

    Google Scholar 

  19. Schenk, G.J., Werkman, T., Wadman, W., Veldhuisen, B., Dijkmans, T.F., Blaas, E., Kegel, L., de Kloet, E.R., and Vreugdenhil, E., Over-Expression of the DCLK Gene Transcript CARP Decreases CA3/CA1 Network Excitability, Brain Res., 2010, vol. 1352, pp. 21–34.

    Article  PubMed  CAS  Google Scholar 

  20. Marcuccilli, C.J., Mathur, S.K., Morimoto, R.I., and Miller, R.J., Regulatory Differences in the Stress Response of Hippocampal Neurons and Glial Cells after Heat Shock, J. Neurosci., 1996, vol. 16, pp. 478–485.

    PubMed  CAS  Google Scholar 

  21. Cotto, J.J., Fox, S.G., and Morimoto, R.I., HSF1 Granules: a Novel Stress-Induced Compartment of Human Cells, J. Cell Sci., 1997, vol. 110, pp. 2925–2934.

    PubMed  CAS  Google Scholar 

  22. Spanswick, S.C., Ev, J.R., and Sutherland, R.J., Time-Course of Hippocampal Granule Cell Degeneration and Changes in Adult Neurogenesis after Adrenalectomy in Rats, Neurosci., 2011, vol. 8, no. 190, pp. 166–176.

    Article  Google Scholar 

  23. Wossink, J., Karst, H., Mayboroda, O., and Joels, M., Morphological and Functional Properties of Rat Dentate Granule Cells after Adrenalectomy, Neurosci., 2001, vol. 108, no. 2, pp. 263–272.

    Article  CAS  Google Scholar 

  24. Galvan, V. and Bredesen, D.E., Neurogenesis in the Adult Brain: Implications for Alzheimer’s Disease, CNS & Neurological Disorders-Drug Targets, 2007, vol. 6, pp. 303–310.

    Article  CAS  Google Scholar 

  25. Huang, Y. and Kandel, E., Recruitment of Long-Lasting and Protein Kinase A-Dependent Long-Term Potentiation in the CA1 Region of Hippocampus Requires Repeated Tetanization, Learn. Mem., 1994, vol. 1, no. 1, pp. 74–82.

    PubMed  CAS  Google Scholar 

  26. Sweatt, J., Toward a Molecular Explanation for Long-Term Potentiation, Learn. Mem., 1999, vol. 6, no. 5, pp. 399–416.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to V. A. Chavushyan.

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Original Russian Text © V.A. Chavushyan, I.B. Meliksetyan, J.S. Sarkissyan, H.Y. Stepanyan, Z.A. Avetisyan, K.V. Simonyan, M.A. Danielyan, V.S. Kamenetskii, 2013, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2013, Vol. 49, No. 2, pp. 153–161.

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Chavushyan, V.A., Meliksetyan, I.B., Sarkissyan, J.S. et al. Electrophysiological and morpho-histochemical study of action of adrenalectomy on hippocampal neurons. J Evol Biochem Phys 49, 193–202 (2013). https://doi.org/10.1134/S0022093013020084

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  • DOI: https://doi.org/10.1134/S0022093013020084

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