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Somatostatin-and Neuropeptide Y-Mediated Neurotransmission in Kindling Epileptogenesis

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Kindling 5

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 48))

Summary

It has been shown that the release of somatostatin (SRIF) and neuropeptide Y (NPY) were significantly enhanced in the hippocampus during kindling epileptogenesis. To investigate the neuronal populations involved in this effect and the consequences of enhanced extracellular concentrations of neuropeptides on their receptors, we measured SRIF and NPY-immunoreactivity (IR) and their receptor binding sites during and at different times after electrical kindling of the rat dorsal hippocampus using immunocytochemistry and quantitative receptor autoradiography.

In the hilar region, SRIF and NPY-1R were strongly increased in interneurons of the polymorphic cell layer and in their presumed projections to the outer molecular layer of the dentate gyrus at the preconvulsive stage 2 and after three consecutive tonic-clonic seizures (stage 5). NPY-IR was also markedly increased in type 1 and type 2 basket cells located below the granule cell layer at both stages of kindling. NPY-IR was transiently expressed in the granule cells/mossy fibres after stage 2 and two days but not one week after stage 5. Similar effects were observed in the hippocampus ipsi-and contralateral to the electrical stimulation and in its septal and temporal poles. The intensity of these changes was similar two days after stages 2 or 5 of kindling, but the effects were less pronounced one week and one month after complete kindling. After a single afterdischarge (AD), peptide-IR was similar to shams except for a transient increase in NPY in the mossy fibres.

During and after kindling, there was a significant decrease (about 40%) in SRIF receptor binding sites in the molecular layer of the dentate gyrus as determined using SRIF1 receptor-selective and non-selective ligands. No changes were observed in the brain of rats after a single AD. Binding to NPY-Y1 receptors was not significantly modified by kindling, while NPY-Y2, receptor binding rose significantly—by 220%—in the terminal field of mossy fibres. This effect was still observed one month after the last stage 5 seizure.

These results are discussed in relation to the functional consequences of changes in neuropeptide-mediated neurotransmission and their possible involvement in the establishment of a chronic epileptic focus.

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References

  1. Bendotti, C., Vezzani, A., Tarizzo, G. and Samanin, R., Increased expression of GAP-43, somatostatin and neuropeptide Y mRNA in the hippocampus during development of hippocampal kindling in rats, Eur J. Neurosci., 5 (1993) 1312–1320.

    Article  PubMed  CAS  Google Scholar 

  2. Brooks, P.A., Kelly, J.S., Allen, J.M., Smith, D.A.S. and Stone, T.W., Direct excitatory effects of neuropeptide Y (NPY) on rat hippocampal neurons in vitro, Brain Res., 408 (1987) 295–298.

    Article  PubMed  CAS  Google Scholar 

  3. Colmers, W.F., Modulation of synaptic transmission in hippocampus by neuropeptide Y: presynaptic actions. In J.M. Allen and J.I. Koenig (Eds.) Central and Peripheral Significance of Neuropeptide Y and its Related Peptides, Ann.NY Acad.Sci„ New York, 1990, pp. 206–218.

    Google Scholar 

  4. Colmers, W.F., Klapstein, G.J., Fournier, A., St-Pierre, S.and Treharne, K.A., Presynaptic inhibition by neuropeptide Y in rat hippocampal slice in vitro is metiated by a Y2 receptor, Br. J. Pharmacol., 102 (1991) 1–44.

    Article  Google Scholar 

  5. DeLanerolle, N.C., Kim, J.H., Robbins, R.J. and Spencer, D.D., Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy, Brain Res., 495 (1989) 387–395.

    Article  CAS  Google Scholar 

  6. Dumont, Y., Fournier, A., St.-Pierre, S. and Quirion, R., Comparative characterization and autoradiographic distribution of neuropeptide Y receptor subtypes in the rat brain, J. Neurosci., 13 (1993) 73–86.

    PubMed  CAS  Google Scholar 

  7. Greber, S., Schwarzer, C. and Sperk, G., Neuropeptide Y inhibits potassium-stimulated glutamate release through Y2 receptors in rat hippocampal slices in vitro, Br. J. Pharmacol., 113 (1994) 737–740.

    Article  PubMed  CAS  Google Scholar 

  8. Hoyer, D., Bell, G.I., Berelowitz, M., Feniuk, W., Humphrey, P.P.A., O’Carroll, A.M. and Patel, Y.C., Classification and nomenclature of somatostatin receptors,TiPS,16 (1995) 86–88.

    CAS  Google Scholar 

  9. Jones, R.S.G., Entorhinal-hippocampal connections: a speculative view of their function, TINS, 16 (1993) 58–64.

    PubMed  CAS  Google Scholar 

  10. Kohler, C., Eriksson, L., Davis, S. and Chan-Palay, V., Co-localization of neuropeptide tyrosine and somatostatin immunoreactivity in neurons of individual subfields of the rat hippocampal region, Neurosci. Lett., 78 (1987) 1–6.

    Article  PubMed  CAS  Google Scholar 

  11. McNamara, J.O., Cellular and molecular basis of epilepsy, J. Neurosci., 14 (1994) 3413–3425.

    PubMed  CAS  Google Scholar 

  12. Milner, T.A. and Bacon, C.E., Ultrastructural localization of somatostatin-like immunoreactivity in the rat dentate gyrus, J. comp. Neural., 290 (1989) 544–560.

    Article  CAS  Google Scholar 

  13. Monno, A., Rizzi, M., Samanin, R. and Vezzani, A., Anti-somatostatin antibody enhances the rate of hippocampal kindling in rats, Brain Res., 602 (1993) 148–152.

    Article  PubMed  CAS  Google Scholar 

  14. Nitsch, R. and Leranth, C., Neuropeptide Y (NPYè-immunoreactive neurons in the primate fascia dentata: occasional coexistence with calcium-binding proteins: a light and electron microscopic study, J. comp. Neurol., 309 (1991) 430–444.

    Article  PubMed  CAS  Google Scholar 

  15. Paxinos, G. and Watson, C., The rat stereotaxic atlas, Academic Press, New York, 1986

    Google Scholar 

  16. Peréz, J., Vezzani, A., Civenni, G., Tutka, P., Rizzi, M., Schupbach, E. and Hoyer, D., Functional effects of D-Phe-c-(Cys-Tyr-D-Trp-Lys-Val-Cys)-Trp-NH, and differential changes in somatostatin receptor messenger RNAs, binding sites and somatostatin release in kainic acid-treated rats, Neuroscience, 65 (1995) 1087–1097.

    Article  PubMed  Google Scholar 

  17. Piwko, C., Thoss, V.S., Samanin, R., Hoyer, D. and Vezzani, A., Changes in somatostatin receptor messenger RNAs and binding sites in rat brain during kindling epileptogenesis (submitted).

    Google Scholar 

  18. Racine, R.J., Modification of seizure activity by electrical stimulation. 11. Motor seizure,Electroenceph. clin. Neurophysiol., 32 (1972) 281–294.

    Article  PubMed  CAS  Google Scholar 

  19. Rizzi, M., Monno, A., Samanin, R., Sperk, G. and Vezzani, A., Electrical kindling of the hippocampus is associated with functional activation of neuropeptide Y-containing neurons, Ear. J. Neurosci., 5 (1993) 1534–1538.

    Article  CAS  Google Scholar 

  20. Robbins, R.J., Brines, M.L., Kim, J.H., Adrian, T., deLanerolle, N., Welsh, M.S. and Spencer, D.D., A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy, Ann. Neurol., 29 (1991) 325–332.

    Article  PubMed  CAS  Google Scholar 

  21. Roder, C., Schwarzer, C., Vezzani, A., Gobbi, M., Mennini, T. and Sperk, G., Autoradiographic analysis of neuropeptide Y receptor binding sites in the rat hippocampus after kainic acid-induced limbic seizures, Neuroscience, 70 (1996) 47–55.

    Article  PubMed  CAS  Google Scholar 

  22. Scharfman, H.E., Presynaptic and postsynaptic actions of somatostatin in area CAl and the dentate gyrus of rat and rabbit hippocampal slices. In T.V. Dunwiddie and D.M. Lovinger (Eds.) Presynaptic Receptors in the Mammalian Brain, Birkhauser, Boston, 1993, pp. 42–70.

    Chapter  Google Scholar 

  23. Schwarzer, C., Sperk, G., Samanin, R., Rizzi, M., Gariboldi, M. and Vezzani, A., Neuropeptides-immunoreactivity and their mRNA expression in kindling: functional implications for limbic epileptogenesis, Brain Res. Rev, (1996) (In press)

    Google Scholar 

  24. Schwarzer, C., Williamson, J.M., Lothman, E.W., Vezzani, A. and Sperk, G., Somatostatin, neuropeptide Y, neurokinin B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy, Neuroscience, 69 (1995) 831–845.

    Article  PubMed  CAS  Google Scholar 

  25. Sloviter, R.S. and Nilaver, G., Immunocytochemical localization of GABA- cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat, J. comp. Neurol., 256 (1987) 42–60.

    Article  PubMed  CAS  Google Scholar 

  26. Sperk, G., Marksteiner, J., Gruber, B., Bellman, R., Mahata, M. and Ortler, M., Functional changes in neuropeptide Y and somatostatin containing neurons induced by limbic seizures in the rat, Neuroscience,50 (1992) 831–846.

    Article  PubMed  CAS  Google Scholar 

  27. Sternberger, L., Immunocytochemistry, Wiley, New York, 1979.

    Google Scholar 

  28. Vezzani, A., Civenni, G., Rizzi, M., Galli, A., Barrios, M. and Samanin, R., Enhanced neuropeptide Y release in the hippocampus is associated with chronic seizure susceptibility in kainic acid treated rats, Brain Res.,660 (1994) 138–143.

    Article  PubMed  CAS  Google Scholar 

  29. Vezzani, A., Monno, A., Rizzi, M., Galli, A., Barrios M. and Samanin, R., Somatostatin release is enhanced in the hippocampus of partially and fully kindled rats, Neuroscience, 51 (1992) 41–46.

    Article  PubMed  CAS  Google Scholar 

  30. Vezzani, A., Serafini, R., Stasi, M.A., Vigano’, G., Rizzi, M. and Samanin, R., Somatostatin and its octapeptide analog SMS 201–995 modulate seizures induced by quinolinic and kainic acids differently in the rat hippocampus, Neuropharmacology,30 (1991) 345–352.

    Article  PubMed  CAS  Google Scholar 

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Vezzani, A., Piwko, C., Gobbi, M., Schwarzer, C., Sperk, G., Hoyer, D. (1998). Somatostatin-and Neuropeptide Y-Mediated Neurotransmission in Kindling Epileptogenesis. In: Corcoran, M.E., Moshé, S.L. (eds) Kindling 5. Advances in Behavioral Biology, vol 48. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5375-5_23

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  • DOI: https://doi.org/10.1007/978-1-4615-5375-5_23

  • Publisher Name: Springer, Boston, MA

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