Epilepsy Research
Volume 26, Issue 2 , Pages 315-327 , January 1997

Decrease in somatostatin-immunoreactive neurons in the rat amygdaloid complex in a kindling model of temporal lobe epilepsy

  • Jarkko Tuunanen

      Affiliations

    • Department of Neurology, University of Kuopio, P.O. Box 1627, FIN-70211 Kuopio, Finland
    • A.I. Virtanen Institute, University of Kuopio, P.O. Box 1627, FIN-70211 Kuopio, Finland
    • ,
  • Toivo Halonen

      Affiliations

    • A.I. Virtanen Institute, University of Kuopio, P.O. Box 1627, FIN-70211 Kuopio, Finland
    • ,
  • Asla Pitkänen

      Affiliations

    • A.I. Virtanen Institute, University of Kuopio, P.O. Box 1627, FIN-70211 Kuopio, Finland
    • Corresponding Author InformationCorresponding author. Tel.: 358 17 163296; fax: 358 17 163025; e-mail: apitkane@messi.uku.fi

Received 22 May 1996 ,Revised 30 July 1996 ,Accepted 6 August 1996.

References 

  1. Aggleton, J.P., The contribution of the amygdala to normal and abnormal emotional states. TINS, 16 (1993) 328–333.
  2. Amaral, D.G., Price, J.L., Pitkänen, A. and Carmichael, S.T., Anatomical organization of the primate amygdaloid complex. In: J.P. Aggleton (Ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfuction, Wiley-Liss, New York, 1992, pp. 339–351.
  3. Babb, T.L., Pretorius, J.K., Kupfer, W.R. and Crandall, P.H., Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J. Neurosci., 9 (1989) 2562–2574.
  4. Babb, T.L. and Pretorius, J.K., Pathologic substrates of epilepsy. In: E. Wyllie, (Ed.), The Treatment of Epilepsy: Principles and Practice, Lea and Febiger, Philadelphia, 1993, pp. 55–70.
  5. Baram, T.Z. and Ribak, C.E., Peptide-induced infant status epilepticus causes neuronal death and synaptic reorganization. NeuroReport, 6 (1995) 277–280.
  6. Bruton, C.J., The neuropathology of temporal lobe epilepsy. In: G. Russel, E. Marley and P. Williams (Eds.), Inst. Psych. Maudsley Monographs, Vol 31, Oxford UP, Oxford, 1988, pp. 195–210.
  7. Callahan, P.M., Paris, J.M., Cunningham, K.A. and Shinnick-Gallagher, P., Decrease of GABA-immunoreactive neurons in the amygdala after electrical kindling in the rat. Brain Res., 555 (1991) 335–339.
  8. Cavazos, J.E. and Sutula, T., Progressive neuronal loss induced by kindling: a possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis. Brain Res., 527 (1990) 1–6.
  9. 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.
  10. Cendes, F., Andermann, F., Gloor, P., Gambardella, A., Lopes-Cendes, I., Watson, C., Evans, A., Carpenter, S. and Olivier, A., Relationship between atrophy of the amygdala and ictal fear in temporal lobe epilepsy. Brain, 117 (1994) 739–746.
  11. Clifford, D.B., Cavalheiro, E.A., Sieklucka-Dziuba, M., Ikonomidou-Turski, C., Czuczwar, S.J. and Turski, L., The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures. Neuroscience, 23 (1987) 953–968.
  12. Dam, M., Epilepsy and neuron loss in the hippocampus. Epilepsia, 21 (1980) 617–629.
  13. Davenport, C.J., Brown, W.J. and Babb, T.L., GABAergic neurons are spared after intrahippocampal kainate in the rat. Epilepsy Res., 5 (1990) 28–42.
  14. Davis, M., The role of the amygdala in conditioned fear. In: J.P. Aggleton, (Ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, Wiley-Liss, New York, 1992, pp. 255–305.
  15. de Lanerolle, 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.
  16. Engel Jr., E., Wolfson, L. and Brown, L., Anatomical correlates of electrical and behavioral events related to amygdaloid kindling. Ann. Neurol., 3 (1978) 538–544.
  17. Fujikawa, D.G. and Hideo, H., Status epilepticus-induced brain damage in humans. Epilepsia, 35 (1994) [Suppl. 9] 8.
  18. Gean, P-W., Shinnick-Gallagher, P. and Anderson, A.C., Spontaneous epileptiform activity and alteration of GABA- and of NMDA-mediated neurotransmission in amygdala neurons kindled in vivo. Brain Res., 494 (1989) 177–181.
  19. Gloor, P., Role of the amygdala in temporal lobe epilepsy. In: J.P. Aggleton, (Ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, Wiley-Liss, New York, 1992, pp. 505–538.
  20. Goddard, G.V., McIntyre, D.C. and Leech, C.K., A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol., 25 (1969) 295–330.
  21. Hosford, D.A., Simonato, M., Cao, Z., Garcia-Cairasco, N., Silver, J.M., Butler, L., Shin, C. and McNamara, J.O., Differences in anatomic distribution of immediately-early gene expression in amygdala and angular bundle kindling development. J. Neurosci., 15 (1995) 2513–2523.
  22. Houser, C.R., Miyashiro, J.E., Swartz, B.E., Walsh, G.O., Rich, J.R. and Delgado-Escueta, A.V., Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10 (1990) 267–282.
  23. Houser, C.R. and Obenaus, A., Hippocampal neurons loss following pilocarpine-induced seizures in developing rats. Epilepsia, 35 (1994) [Suppl. 8] 9.
  24. Hudson, L.P., Muñoz, D.G., Miller, L., McLachlan, R.S., Girvin, J.P. and Blume, W.T., Amygdaloid sclerosis in temporal lobe epilepsy. Ann. Neurol., 33 (1993) 622–631.
  25. Kato, N., Higuchi, T., Friesen, H.G. and Wada, J.A., Changes of immunoreactive somatostatin and -endorphin content in rat brain after amygdaloid kindling. Life Sci., 32 (1983) 2415–2422.
  26. LeDoux, J.E., Emotion and the Amygdala. In: J.P. Aggleton, (Ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, Wiley-Liss, New York, 1992, pp. 339–351.
  27. Lewis, D.A., Campbell, M.J. and Morrison, J.H., An immunohistochemical characterization of somatostatin-28 and somatostatin 281–12 in monkey prefrontal cortex. J. Comp. Neurol., 212 (1986) 293–312.
  28. Margerison, J.H. and Corsellis, J.A.N., Epilepsy and temporal lobes. A clinical. electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobe. Brain, 89 (1966) 499–530.
  29. McDonald, A.J. and Pearson J.C., Coexistence of GABA and peptide immunoreactivity in non-pyramidal neurons of the basolateral amygdala. Neurosci. Lett., 100 (1989) 53–58.
  30. Miller, L.A., McLachlan, R.S., Bouwer, M.S., Hudson, L.P. and Muñoz, M.G., Amygdalar sclerosis: preoperative indicators and outcome after temporal lobe lobectomy. J. Neurol. Neurosurg. Psychiatry, 57 (1994) 1099–1105.
  31. Nitecka, L. and Ben-Ari, Y., Distribution of GABA-like immunoreactivity in the rat amygdaloid complex. J. Comp. Neurol., 266 (1987) 45–55.
  32. Obenaus, A., Esclapez, M. and Houser, C., Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J. Neurosci., 13 (1993) 4470–4485.
  33. Paxinos, G. and Watson, C., The rat brain stereotaxic coordinates. Academic Press, New York, 1986.
  34. Pinel, J.P.J., Mucha, R.F. and Phillips, A.G., Spontaneous seizures generated in rats by kindling: A preliminary report. Physiol. Psychol., 3 (1975) 127–129.
  35. Pitkänen A., Tuunanen J. and Halonen T., Vigabatrin and carbamazepine have different efficacies in the prevention of status epilepticus induced neuronal damage in the hippocampus and amygdala. Epilepsy Res., 24 (1996) 29–45.
  36. Price, J.L., Russchen, F.T. and Amaral, D.G., The limbic region. II: The amygdaloid complex. In: A. Björklund, T. Hökfelt, L.W. Swanson (eds.), Handbook of chemical neuroanatomy, Vol 5, Integrated systems of the CNS, Part I., Amsterdam, Elsevier, 1987, pp. 279–388.
  37. Racine, R., Modulation of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol., 32 (1972) 281–294.
  38. Rainnie, D.G., Asprodini, E.K. and Shinnick-Gallagher, P., Kindling-induced long-lasting changes in synaptic transmission in the basolateral amygdala. J. Neurophysiol., 67 (1992) 443–454.
  39. Represa, A., Niquet J., Pollard, H., Khrestchatisky M. and Ben-Ari, Y., From seizures to neo-synaptogenesis: Intrinsic and extrinsic determinants of mossy fiber sprouting in the adult hippocampus. Hippocampus, 4 (1994) 270–274.
  40. Robbins, R.J., Brines, M.L., Kim, J.H., Adrian, T., de Lanerolle, N., Welsh, 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.
  41. Saukkonen, A., Kälviäinen, R., Partanen, K., Vainio, P., Riekkinen, P. and Pitkänen, A., Do seizures cause neuronal damage? A MRI study in newly diagnosed and chronic epilepsy. NeuroReport, 6 (1995) 219–223.
  42. Savander, V., Go, C.-G., LeDoux, J.E. and Pitkänen, A., Intrinsic connections of the rat amygdaloid complex: Projections originating in the basal nucleus. J. Comp. Neurol., 361 (1995) 345–368.
  43. Savander, V., LeDoux, J.E. and Pitkänen, A., Interamygdaloid projections of the basal and accessory basal nuclei of the rat amygdaloid complex. Neuroscience, (1996), in press.
  44. Schwob, J.E., Fuller, T., Price, J.L. and Olney, J.W., Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: A histological study. Neuroscience, 5 (1980) 991–1014.
  45. Shinoda, H., Schwartz, J.P. and Nadi, N.S., Amygdaloid kindling of rats increases preprosomatostatin mRNA and somatostatin without affecting glutamic acid decarboxylase (GAD) mRNA or GAD. Mol. Brain Res., 5 (1989) 243–246.
  46. 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.
  47. Sloviter, R.S., Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science, 235 (1987) 73–76.
  48. 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.
  49. 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.
  50. Sutula, T., Xiao-Xian, H., Cavazos, J. and Scott, G., Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science, 239 (1987) 1147–1150.
  51. Sutula, T., Cascino, G., Cavazos, J., Parada, I. and Ramirez, L., Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol., 26 (1989) 321–330.
  52. Sutula T., Cavazos, J. and Woodard A., Long-term structural and functional alterations induced in the hippocampus by kindling: Implications for memory dysfunction and the development of epilepsy. Hippocampus, 4 (1994) 254–258.
  53. Szabat, E., Soinila, S., Häppölä, O., Linnala, A. and Virtanen, I., A new monoclonal antibody against the GABA-protein conjugate shows immunoreactivity in sensory neurons of the rat. Neuroscience, 47 (1992) 409–420.
  54. 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.
  55. Tuunanen, J., Halonen, T. and Pitkänen, A., Status epilepticus causes selective regional damage and loss of GABAergic neurons in the amygdaloid complex. Eur. J. Neurosci., in press.
  56. White, L.E. and Price, J.L., The functional anatomy of limbic status epilepticus in the rat. I. Patterns of 14C-2-deoxyglucose and FOS immunohistochemistry. J. Neurosci., 13 (1993) 4787–4809.
  57. Äikiä, M., Kälviäinen, R. and Riekkinen, P.J., Verbal learning and memory in newly diagnosed partial epilepsy. Epilepsy Res., 22 (1995) 157–164.

PII: S0920-1211(96)00900-X

doi: 10.1016/S0920-1211(96)00900-X

Epilepsy Research
Volume 26, Issue 2 , Pages 315-327 , January 1997

Article Tools

* Image Usage & Resolution