Neuropeptides-immunoreactivity and their mRNA expression in kindling: Functional implications for limbic epileptogenesis

Brain Research Reviews

Volumn 22, Issue 1, 1996, Pages 27-50

  Schwarzer, Christoph ^b   Sperk, Günther ^b   Samanin, Rosario ^a   Rizzi, Massimo ^a   Gariboldi, Marco ^a   Vezzani, Annamaria ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Dentate gyrus; Hippocampus; Limbic system; Neurodegeneration; Rat; Seizure; Sprouting; Tachykinin; Temporal lobe epilepsy

Indexed keywords

CHOLECYSTOKININ; MESSENGER RNA; NEUROKININ B; NEUROPEPTIDE; NEUROPEPTIDE Y; SOMATOSTATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; EPILEPSY; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; KINDLING; LIMBIC SYSTEM; MALE; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; SEIZURE;

EID: 0002911726     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/0165-0173(96)00005-7     Document Type: Review

References (119)

1. [1] Aitken, P.G., Jaffe, D.B. and Nadler, J.V., Cholecystokinin blocks some effects of kainic acid in CA3 region of hippocampal slices, Peptides, 12 (1991) 127-129.
2. [2] Babb, T.L., Kupfer, W.R., Pretorius, J.K., Crandall, P.H. and Levesque, M.F., Synaptic reorganization by mossy fibers in human epileptic fascia dentata, Neuroscience, 42 (1991) 351-363.
3. [3] Babb, T.L., Mathern, G.W., Leite, J.P. and Pretorius, J.K., GABA-A alpha and beta receptors and GAD-IR axon sprouting in human hippocampal epilepsy, Soc. Neurosci. Abstr., 20 (1994) 592.8.
4. [4] Bakst, I., Avendano, C., Morrison, J.H. and Amaral, D.G., An experimental analysis of the origins of somatostatin-like immunoreactivity in the dentate gyrus of the rat. J. Neurosci., 6 (1986) 1452-1462.
5. [5] Bellmann, R., Widmann, R., Olenik, C., Meyer, D.K., Maas, D., Marksteiner, J. and Sperk G., Enhanced rate of expression and biosynthesis of neuropeptide Y after kainic acid induced seizures, J. Neurochem., 56 (1991) 525-530.
6. [6] Ben-Ari, Y., Limbic seizures and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy, Neuroscience, 14 (1985) 375-403.
7. [7] 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.
8. [8] Bonner, T.I., Affolter, H.-U., Young, A.C. and Young, W.S. III, A cDNA encoding the precursor of the rat neuropeptide, neurokinin B, Mol. Brain Res., 2 (1987) 243-249.
9. [9] Brene, S., Lindefors, N., Ballarin, M. and Persson, H., Kainic acid-mediated increase of preprotachykinin-A messenger RNA expression in the rat hippocampus and a region-selective attenuation by dexamethasone, Neuroscience, 50 (1992) 611-618.
10. [10] 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.
11. [11] Cavazos, J.E., Golarai, G. and Sutula, T.P., Mossy fibre synaptic reorganization induced by kindling: time course of development, progression, and permanence, J. Neurosci., 11 (1991) 2795-2803.
12. [12] Cavazos, J.E., Das, I. and Sutula, T.P., Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures, J. Neurosci., 14 (1994) 3106-3121.
13. 2 receptor, Br. J. Pharmacol., 102 (1991) 41-44.
14. [14] Cronin, J., and Dudek, F.E., Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats, Brain Res., 474 (1988) 181-184.
15. [15] Davenport, C.J., Brown, W.J. and Babb, T.L., Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat, Exp. Neurol., 109 (1990) 180-190.
16. [16] 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.
17. [17] Deller, T. and Leranth, C., Synaptic connections of neuropepitide Y (NPY) immunoreactive neurons in the hilar area of the rat hippocampus, J. Comp. Neurol., 300 (1990) 433-447.
18. [18] Deschenes, R.J., Lorenz, L.J., Haun, R.S., Roos, B.A., Collier, K.J. and Dixon, J.E., Cloning and sequence analysis of cDNA encoding rat preprocholecystokinin, Proc. Natl. Acad. Sci. USA, 81 (1984) 726-730.
19. [19] Esclapez, M. and Houser, C.R., Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: evidence from colocalization of pre-prosomatostatin and glutamate decarboxylase messenger RNAs, Neuroscience, 64 (1995) 339-355.
20. [20] Fredens, K., Stengaard-Pedersen, K. and Larsson, L.-L., Localization of enkephalin and cholecystokinin immunoreactivities in the perforant path terminal field of the rat hippocampal formation, Brain Res., 304 (1984) 255-263.
21. [21] Fredens, K., Stengaard-Pedersen, K. and Wallace, M.N., Localization of cholecystokinin in the dentate commissural-associational system of the mouse and rat, Brain Res., 401 (1987) 68-78.
22. [22] Gall, C. and Selawski, L., Supramammillary afferents to guinea pig hippocampus contain substance P-like immunoreactivity, Neurosci. Lett., 51 (1984) 171-176.
23. [23] Gall, C., Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and CCK immunoreactivities in mouse hippocampal mossy fibers, J. Neurosci., 8 (1988) 1852-1862.
24. [24] Gall, C., Lauterborn, J., Isackson, P. and White, J., Seizures, neuropeptide regulation, and mRNA expression in the hippocampus, Prog. Brain Res., 83 (1990) 371-390.
25. [25] Goddard, G.V., McIntyre, D.C. and Leech, C.K., A permanent change in brain function resulting from daily electrical stimulation, Expl. Neurol., 25 (1969) 295-330.
26. 2 receptors in rat hippocampal slices in vitro, Br. J. Pharmacol, 113 (1994) 737-740.
27. [27] Greenwood, R.S., Godar, S.E., Reaves, T.A. Jr. and Hayward, J.N., Cholecystokinin in hippocampal pathways, J. Comp. Neurol., 203 (1981) 335-350.
28. [28] Grüber, B., Greber, S. and Sperk, G., Kainic acid seizures cause enhanced expression of cholecystokinin-octapeptide in the cortex and hippocampus of the rat, Synapse, 15 (1993) 221-228.
29. [29] Grüber, B., Greber, S., Rupp, E. and Sperk, G., Differential NPY mRNA expression in granule cells and interneurons of the rat dentate gyrus after kainic acid, Hippocampus, 4 (1994) 1-9.
30. [30] Harris, K.M., Marshall, P.E. and Landis, D.M.D., Ultrastructural study of cholecystokinin-immunoreactive cells and processes in area CA1 of the rat hippocampus, J. Comp. Neurol., 233 (1985) 147-158.
31. [31] Harrison, M.B., Shumate, M.D. and Lothman, E.W., Opioid peptide expression in models of chronic temporal lobe epilepsy, Neuroscience, 65 (1995) 785-795.
32. [32] Hashimoto, T. and Obata, K., Induction of somatostatin by kainic acid in pyramidal and granule cells of the rat hippocampus, Neurosci. Lett., 12 (1991) 514-527.
33. [33] Hökfelt, T., Johansson,O., Ljungdahl, A., Lundberg, J.M. and Schultzberg, M., Peptidergic neurones, Nature, 284 (1980) 515-521.
34. [34] Hökfelt, T., Neuropeptides in perspective: the last ten years, Neuron, 7 (1991) 867-879.
35. [35] Hong, J.S., Wood, P.L., Gillin, J.C., Yang, H.Y.T. and Costa, E., Changes of hippocampal met-enkephalin content after recurrent motor seizures, Nature, 285 (1980) 231-232.
36. [36] Hong, J.S., McGinty, J.F., Lee, P.H.K., Xie, C.W. and Mitchell, C.L., Relationship between hippocampal opioid peptides and seizures, Prog. Neurobiol., 40 (1993) 507-528.
37. [37] Iadarola, M.J., Shin, C., McNamara, J.O. and Yang, H.-Y.T., Changes in dynorphin, enkephalin and cholecystokinin content of hippocampus and substantia nigra after amygdala kindling, Brain Res., 365 (1986) 185-191.
38. [38] Johansen, F.F., Tonder, N., Bruhn, T. and Diemer, N.H., Neuropeptide Y immunoreactivity is lost in rat hippocampus after cerebral ischemia and kainic acid seizures, Eur. J. Neurosci., Suppl. 2 (1989) 13.
39. [39] Kadar, T., Pesti, A., Penke, B., Toth, G., Zarandi, M. and Teledgy, G., Structure activity and dose effect relationships of the antagonism of picrotoxin induced seizures by cholecystokinin fragments and analogs of cholecystokinin in mice, Neuropharmacology, 22 (1983) 1223-1230.
40. 5-enkephalin and the level of dynorphin A in the rat hippocampus, J. Neurosci., 6 (1986) 3094-3102.
41. [41] Kato, N., Higuchi, T., Friesen, H.G. and Wada, J.A., Changes of immunoreactive somatostatin and β-endorphin content in rat brain after amygdaloid kindling, Life Sci., 32 (1983) 2415-2422.
42. [42] Köhler, C., Chan-Palay, V., Somatostatin-like immunoreactive neurons in the hippocampus: an immunocytochemical study in the rat. Neurosci., Lett., 34 (1982) 259-264.
43. [43] Köhler, C., Eriksson, L., Davies, S. and Chan-Palay, V., Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain, J. Comp. Neurol., 244 (1986) 384-400.
44. [44] Köhler, C., Eriksson, L.G., Davies, 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.
45. [45] Kosaka, T., Kosaka, K., Tateishi, K., Hamaoka, Y., Yanaihara, N., Wu, J.-Y. and Hama, K., GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus, J. Comp. Neurol., 139 (1985) 420-430.
46. [46] Kosaka, T., Wu, J.-Y. and Benoit, R., GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus, Exp. Brain Res., 71 (1988) 388-398.
47. [47] Lanaud, P., Popovici, T., Normand, E., Lemoine, C., Bloch, B. and Roques, B.P., Distribution of CCK mRNA in particular regions (hippocampus, periaqueductal grey and thalamus) of the rat by in situ hybridization, Neurosci. Lett., 104 (1989) 38-42.
48. [48] Larhammar, D., Ericsson, A. and Persson, H., Structure and expression of the rat neuropeptide Y gene, Proc. Natl. Acad. Sci. USA, 84 (1987) 2068-2072.
49. [49] Lason, W., Przewlocka, B. and Przewlocki, R., The prodynorphin system in the rat hippocampus is differentially influenced by kainic acid and pentetrazole, Neuroscience. 51 (1992) 357-362.
50. [50] Laurberg, S. and Sorensen, K.E., Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3), Brain Res., 212 (1981) 287-300.
51. [51] Leranth, C. and Frotscher, M., Synaptic connections of cholecystokinin-immunoreactive neurons and terminals in the rat fascia dentata: a combined light and electron microscopic study. J. Comp. Neurol., 254 (1986) 51-64.
52. [52] Leranth, C., Malcolm, A.J. and Frotscher, M., Afferent and efferent synaptic connections of somatostatin-immunoreactive neurons in the rat fascia dentata, J. Comp. Neurol., 295 (1990) 111-122
53. [53] Leung, L.S., Spontaneous hippocampal interictal spikes following local kindling: time course of changes and relation to behavioral seizures, Brain Res., 513 (1990) 308-314.
54. [55] Lothman, E.W., Bertram, E.H. III and Stringer, J.L., Functional anatomy of hippocampal seizures, Prog. Neurobiol., 37 (1991)1-81.
55. [56] Lothmam, E.W. and Bertram, E.H., III, Epileptogenic effects of status epilepticus. Epilepsia. 34 (1993) S59-S70.
56. 27-33), Brain Res., 406 (1987) 130-135.
57. [58] Mahata, S.K., Marksteiner, J., Sperk, G., Mahata, M., Gruber, B., Fischer-Colbrie, R. and Winkler, H., Temporal lobe epilepsy of the rat: differential expression of mRNAs of chromogranin B, secretogranin II, synaptin/synaptophysis and p65 in subfields of the hippocampus. Mol. Brain Res., 16 (1992) 1-12.
58. [59] Mahata, S.K., Grüber, B., Mahata, M., Roder, C., Fischer-Colbrie, R. and Sperk, G., Kainic acid seizures in the rat: differential expression of chromogranin A, carboxypeptidase H and peptidylglycine α-amidating monooxygenase in subfields of the hippocampal formation, Acta Neuropathol., 86 (1993) 590-595.
59. [60] Mancillas, J.R., Siggins, G.R. and Bloom, F.E., Somatostatin selectively enhances acetylcholine-induced excitations in rat hippocampus and cortex, Proc. Natl. Acad. Sci. USA, 83 (1986) 7518-7521.
60. [61] Manfridi, A., Forloni, G.L., Vezzani, A., Fodritto, F., De Simoni, M.G., Functional and histological consequences of quinolinic and kainic acid-induced seizures on hippocampal somatostatin neurons, Neuroscience, 41 (1991) 127-135.
61. [62] Marksteiner, J. and Sperk, G., Concomitant increase of somatostatin, neuropeptide Y and glutamate decarboxylase in the frontal cortex of rats with decreased seizure threshold, Neuroscience, 26 (1988) 379-385.
62. [63] Marksteiner, J., Sperk, G., Maas, D., Differential increases in brain levels of neuropeptide Y and vasoactive intestinal polypeptide after kainic acid-induced seizures in the rat, Naunyn-Schmiedeberg's Arch. Pharmacol., 339 (1989) 173-177.
63. [64] Marksteiner, J., Sperk, G., Krause, J.E., Distribution of neurons expressing neurokinin B in the rat brain: immunohistochemistry and in situ hybridization, J. Comp. Neurol., 317 (1992) 341-356.
64. [65] Marksteiner, J., Wahler, R., Bellmann, R., Ortler, M., Krause, J.E. and Sperk, G., Limbic seizures cause pronounced changes in the expression of neurokinin B in the hippocampus of the rat, Neuroscience. 49 (1992) 383-395.
65. [66] Mazarati, A.M. and Teledgy, G., Effects of somatostatin and anti-somatostatin serum on picrotoxin-kindled seizures, Neuropharmacology, 31 (1992) 793-797.
66. [67] McNamara, J.O., Kindling: an animal model of complex partial epilepsy, Ann. Neurol., 16 (Suppl) (1984) S72-S76.
67. [68] McNamara, J.O., Cellular and molecular basis of epilepsy, J. Neurosci., 14 (1994) 3413-3425.
68. [69] Meyer, D.K., Widmann, R., Sperk, G., Increased brain levels of cholecystokinin octapeptide after kainic acid-induced seizures in the rat. Neurosci. Lett.. 69 (1986) 208-211.
69. 3H)GABA from slices of rat caudatoputamen, Neuroscience, 28 (1989) 61-68.
70. [71] Mikkelsen, J.D., Woldbye, D., Kragh, J., Larsen, P.J. and Bolwig, T.G., Electroconvulsive shocks increase the expression of neuropeptide Y (NPY) mRNA in the piriform cortex and the dentate gyrus. Mol. Brain Res., 23 (1994) 317-322.
71. [72] Milner, T.A., Bacon, C.E., Ultrastructural localization of somatostatin-like immunoreactivity in the rat dentate gyrus, J. Comp. Neurol., 290 (1989) 544-560.
72. [73] Mitchell, J., Gatherer, M. and Sundstrom, L.E., Loss of hilar somatostatin neurons following tetanus toxin-induced seizures, Acta Neuropathol., 89 (1995) 425-430.
73. [74] Monnet, F.P., Fournier, A., Debonnel, G. and de Montigny, C., Neuropeptide Y potentiates response in the CA3 dorsal hippocampus. I. Involvement of an atypical neuropeptide Y receptor, J. Pharmacol. Exp. Ther., 263 (1992) 1212-1218.
74. [75] 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.
75. [76] Morris, B.J., Feasey, K.J., Bruggencate, G.T., Herz, A. and Hollt, V., Electrical stimulation in vivo increases the expression of proenkephalin mRNA and decreases the expression of prodynorphin mRNA in rat hippocampal granule cells, Proc. Natl. Acad. Sci USA, 85 (1988) 3226-3230.
76. [77] Nitsch, R. and Leranth, C., Neuropeptide Y (NPY)-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.
77. [78] Nunzi, M.G., Gorio, A., Milan, F., Freund, T.F., Somogy, P. and Smith, A.D., Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus, J. Comp. Neurol., 237 (1985) 485-505.
78. [79] Olenik, C., Meyer, D.K., Marksteiner, J. and Sperk, G., Concentrations of mRNAs encoding for preprosomatostatin and preprocholecystokinin are increased after kainic acid-induced seizures, Synapse, 4 (1989) 223-228.
79. 2 and differential changes in somatostatin receptor messenger RNAs. binding sites and somatostatin release in kainic acid-treated rats. Neuroscience. 65 (1995) 1087-1097.
80. [81] Pitkanen, A., Sirvio, J., Jolkkonen, J. and Riekkinen, P., Somatostatin-like immunoreactivity and somatostatin receptor binding in rat brain before and after pentylenetetrazole-induced convulsion, Neuropeptides, 7 (1986) 63-71.
81. [82] Racine, R.J., Modification of seizure activity by electrical stimulation. II. Motor seizure, Electroenceph. Clin. Neurophysiol. 32 (1972) 281-294.
82. [83] Represa, A., Le Gall La Salle, G., Ben-Ari, Y., Hippocampal plasticity in the kindling model of epilepsy in rats. Neurosci. Lett., 99 (1989) 345-350.
83. [84] 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. Eur. J.Neuroscience, 5 (1993) 1534-1538.
84. [85] 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.
85. [86] Röder, C., Schwarzer, C., Vezzani, A., Gobbi, M., Mennini, T. and Sperk, G., Autoradiographic analysis of neuropeptide Y binding sites in the rat hippocampus after kainic acid-induced limbic seizures. Neuroscience, 70 (1996) 47-55.
86. [87] Rosen, J.B., Cain, C.J., Weiss, S.R.B. and Post, R.M., Alterations in mRNA of enkephalin, dynorphin and thyrotropin releasing hormone during amygdala kindling: an in situ hybridization study. Mol. Brain Res., 15 (1992) 247-255.
87. [88] Scharfman, H.E. and Schwartzkroin, P.A., Responses of cells of the rat fascia dentata to prolonged stimulation of the perforant path: sensitivity of hilar cells and changes in granule cell excitability. Neuroscience. 35 (1990) 491-504.
88. [89] Scharfman, H.E., Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J. Neurosci., 11 (1991) 1660-1673.
89. [90] Scharfman, H.E., Presynaptic and postsynaptic actions of somatostatin in area CA1 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.
90. [91] Scharfman, H.E., EPSPs of dentate gyrus granule cells during epileptiform bursts of dentate hilar 'mossy' cells and area CA3 pyramidal cells in disinhibited rat hippocampal slices, J. Neurosci., 14 (1994) 6041-6057.
91. [92] 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.
92. [93] Segal, M., A potent inhibitory monosynaptic hypothalamo-hippocampal connection. Brain Res., 162 (1979) 137-141.
93. [94] Seress, L. and Ribak, C.E., GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp. Brain Res., 50 (1983) 173-182.
94. [95] Shinoda, H., Nadi, N.S. and Schwartz, J.P., Alterations in somatostatin and proenkephalin mRNA in response to a single amygdaloid stimulation versus kindling. Mol. Brain Res., 11 (1991) 221-226.
95. [96] Shinohara, S., Katsuura, G., Eigyo, M., Shintaku, H., Ibii, N. and Matsushita, A., Inhibitory effects of CCK-8 and ceruletide on glutamate-induced rises in intracellular free calcium concentrations in rat neuron cultures. Brain Res., 588 (1992) 223-228.
96. [97] Sinton, C.M., Cholecystokinin modulates neurotransmission through the dentate gyrus, Neurosci. Lett., 95 (1988) 341-346.
97. [98] Sloviter, R.S., Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science, 235 (1987) 73-76.
98. [99] 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.
99. [100] Sloviter, R.S., Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the 'dormant basket cell' hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus, 1 (1991) 41-66.
100. [101] Sloviter, R.S. and Lowenstein, D.H., Heat shock protein expression in vulnerable cells of the rat hippocampus as an indicator of excitation-induced neuronal stress. J. Neurosci., 12 (1992) 3004-3009.
101. [102] Sloviter, R.S., The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy, Ann. Neurol., 35 (1994) 640-654.
102. [103] Somogyi, P., Hodgson, A.J., Smith, A.D., Nunzi, M.G., Gorio, A. and Wu, J.-Y., Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin-or cholecystokinin-immunoreactive material. J. Neurosci., 4 (1984) 2590-2603.
103. [104] Sperk, G. and Widmann, R., Somatostatin precursor in the rat striatum: changes after local injection of kainic acid, J. Neurochem., 45 (1985) 1441-1447.
104. [105] Sperk, G., Wieser, R., Widmann, R. and Singer, E.A., Kainic acid induced seizures: Changes in somatostatin, substance P and Neurotensin, Neuroscience, 17 (1986) 1117-1126.
105. [106] Sperk, G., Marksteiner, J., Gruber, B., Bellmann, 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.
106. [107] Sperk, G., Kainic acid seizures in the rat. Prog. Neurobiol., 42 (1994) 1-32.
107. [108] Sternberger, L., Immunohistochemistry, 2nd ed., Wiley, New York, 1979.
108. [109] Stringer, J. and Lothman, E.W., Bilateral maximal dentate activation is critical for the appearance of an afterdischarge in the dentate gyrus. Neuroscience. 46 (1992) 309-314.
109. [110] Sutula, T., Xian, H.X., Cavazos, J. and Scott, G., Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science. 239 (1988) 1147-1150.
110. [111] Tauck, D.L. and Nadler, J.V., Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats, J. Neurosci., 5 (1985) 1016-1022.
111. [112] Tavianini, M.A., Hayes, I.E., Magazin, M,D., Minth, C.D. and Dixon, J.E., Isolation, characterization, and DNA sequence of the rat somatostatin gene, J. Biol. Chem, 259 (1984) 11798-11803.
112. [113] Vezzani, A., Wu, H.Q., Moneta, E. and Samanin, R., Role of the N-methyl-D-aspartate-type receptors in the development and maintenance of hippocampal kindling in rats, Neurosci. Lett, 87 (1988) 63-68.
113. [114] Vezzani, A., Serafini, R., Stasi, M.A., Viganó, 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.
114. [115] 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.
115. [116] Vezzani, A., Civenni, G., Rizzi, M., Monno, A., Messali, S. 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.
116. [117] Wanscher, B., Kragh, J., Barry, D.I., Bolwig, T. and Zimmer, J., Increased somatostatin and enkephalin-like immunoreactivity in the rat hippocampus following hippocampal kindling, Neurosci. Lett., 118 (1990) 33-36.
117. [118] Ylinen, A., Valjakka, A., Lahtinen, H., Miettinen, R., Freund, T.F. and Riekkinen, P., Vigabatrin pre-treatment prevents hilar somatostatin cell loss and the development of interictal spiking activity following sustained stimulation of the perforant path, Neuropeptides, 19 (1991) 205-211.
118. [119] Young III, W.S., In situ hybridization. Histochemical detection of neuropeptide mRNA using DNA and RNA probes, Meth. Enzymol., 168 (1989) 702-709.
119. [120] Zetler, G., Anticonvulsant effects of caerulein, cholecystokinin octapeptide (CCK-8) and diazepam against seizures produced in mice by harman, thiosemicarbazide and isoniazid, Neurosci. Lett., 24 (1981) 175-180.