Epilepsy Research
Volume 26, Issue 1 , Pages 219-231 , December 1996

Neuron loss, mossy fiber sprouting, and interictal spikes after intrahippocampal kainate in developing rats

  • João P. Leite

      Affiliations

    • Corresponding Author InformationCorresponding author. Reed Neurological Research Center, UCLA Medical Center, Los Angeles, CA 90095-1769. Fax: +1 (310) 206-8461.
    • The Brain Research Institute, University of California, Los Angeles, CA, USA
    • Department of Neurology, Ribeirão Preto School of Medicine, University of São Paulo, Ribeirão, São Paulo, Brazil
    • ,
  • Thomas L. Babb

      Affiliations

    • Departments of Neuroscience and Neurology, Cleveland Clinic Foundation, Cleveland, OH, USA
    • ,
  • James K. Pretorius

      Affiliations

    • The Brain Research Institute, University of California, Los Angeles, CA, USA
    • ,
  • Paula A. Kuhlman

      Affiliations

    • The Brain Research Institute, University of California, Los Angeles, CA, USA
    • ,
  • Kristin M. Yeoman

      Affiliations

    • The Brain Research Institute, University of California, Los Angeles, CA, USA
    • ,
  • Gary W. Mathern

      Affiliations

    • The Brain Research Institute, University of California, Los Angeles, CA, USA
    • Department of Neurology, University of California, Los Angeles, CA, USA
    • Division of Neurosurgery, University of California, Los Angeles, CA, USA

Received 26 October 1995 ,Accepted 12 March 1996.

References 

  1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 1946;94:239–247
  2. Albala BJ, Moshè SL, Okada R. Kainic acid-induced seizures: A developmental study. Dev. Brain Res. 1984;13:139–148
  3. Altman J, Bayer S. Postnatal development of the hippocampal dentate gyrus under normal and experimental conditions. In: 2nd ed..  Isaacson RL,  Pribram KH editor. The Hippocampus, Structure and Development. Vol. 1:New York: Plenum; 1975;p. 95–122
  4. Amaral DG, Dent JA. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 1981;195:51–86
  5. Annegers JF, Hauser WA, Elveback LR, Kurkland LT. The risk of epilepsy following febrile convulsions. Neurology. 1979;29:297–303
  6. Annegers JF, Hauser WA, Shirts SB, Kurland LT. Factors prognostic of unprovoked seizures after febrile convulsions. New Engl. J. Med. 1987;316:493–498
  7. Babb TL, Brown MJ. Pathological findings in epilepsy. In:  Engel J editors. Surgical Treatment of the Epilepsies. New York: Raven Press; 1987;p. 511–540
  8. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 1991;42:351–363
  9. Ben-Ari Y, Tremblay E, Berger M, Nitecka L. Kainic acid seizure syndrome and binding sites in developing rats. Dev. Brain Res. 1984;14:284–288
  10. Cherubini E, De Feo MR, Mecarelli O, Ricci GF. Behavioral and electrographic patterns induced by systemic administration of kainic acid in developing rats. Dev. Brain Res. 1983;9:69–77
  11. Cook TM, Crutcher KA. Extensive target cell loss during development results in mossy fibers in the regio superior (CA1) of the rat hippocampal formation. Dev. Brain Res. 1985;21:19–30
  12. Cook TM, Crutcher KA. Intrahippocampal injection of kainic acid produces significant pyramidal cell loss in neonatal rats. Neuroscience. 1986;18:79–92
  13. Cronin J, Obenaus A, Houser CR, Dudek FE. Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res. 1992;573:305–310
  14. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 1989;495:387–395
  15. Dunn DW. Status epilepticus in children: Etiology, clinical features, and outcome. J. Neurol. Child. 1988;3:167–173
  16. Falconer MA. The pathological substrate of temporal lobe epilepsy. Guy's Hosp. Rep. 1970;119:47–60
  17. Gastaut H, Toga M, Roger J, Gibsen WC. A correlation of clinical electroencephalographic and anatomical findings in nine autopsied cases of temporal lobe epilepsy. Epilepsia. 1959;1:56–85
  18. Gotman J. Automatic recognition of epileptic seizures in the EEG. Electroencephalogr. Clin. Neurophysiol. 1982;54:530–540
  19. Holmes GL, Thompson JL. Effects of kainic acid on seizure susceptibility in the developing brain. Dev. Brain Res. 1988;39:51–59
  20. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 1990;10:267–282
  21. Leite JP, Babb TL, Mathern GW, Pretorius JK, Seki T. Axonal growth and terminal specialization of mossy fibers in developing rat pups: An NCAM-H and Neo-Timm's study. Soc. Neurosci. Abstr. 1994;20:1682
  22. Lorente de Nó R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psych. Neurol. 1993;45:113–177
  23. Magloczky ZS, Freund TF. Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience. 1993;56:317–336
  24. Margerison JH, Corsellis JAN. Epilepsy and the temporal lobes. Brain. 1966;89:499–530
  25. Mathern GW, Kupfer WR, Pretorius JK, Babb TL, Levesque MF. Onset and patterns of hippocampal sprouting in the rat kainate seizure model: Evidence for progressive cell loss and neo-innervation in regio inferior and superior. Dendron. 1992;1:69–84
  26. Mathern GW, Cifuentes F, Leite JP, Pretorius JK, Babb TL. Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr. Clin. Neurophysiol. 1993;87:326–339
  27. Mathern GW, Babb TL, Vickery BG, Melendez M, Pretorius JK. Traumatic compared to non-traumatic clinical-pathologic associations in temporal lobe epilepsy. Epilepsy Res. 1994;19:129–139
  28. Mathern GW, Pretorius JK, Babb TL. Quantified patterns of mossy fiber sprouting and neuron densities in hippocampal and lesional seizures. J. Neurosurg. 1995;82:211–219
  29. Mathern GW, Pretorius JK, Babb TL. Influence of the type of initial precipitating injury and at what age it occurs on course and outcome in patients with temporal lobe seizures. J. Neurosurg. 1995;82:220–227
  30. Mathern GW, Babb TL, Vickrey BG, Melendez M, Pretorius JK. The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain. 1995;118:105–118
  31. Maytal J, Shinnar S, Moshé SL, Alvarez LA. The low morbidity and mortality of status epilepticus in children. Pediatrics. 1989;83:323–331
  32. McNamara JO. Cellular and molecular basis of epilepsy. J. Neurosci. 1994;14:3413–3425
  33. Meldrum BS, Vigouroux RA, Brierley JB. Systemic factors and epileptic brain damage. Arch. Neurol. 1973;29:82–87
  34. Moshé SL, Sperber EF, Valisek L. Critical issues of developmental seizure disorders. Physiol. Res. 1993;42:145–154
  35. Nelson KB, Ellenberg JH. Predictors of epilepsy in children who have experienced febrile seizures. New Engl. J. Med. 1976;295:1029–1033
  36. Nitecka L, Tremblay E, Charton G, Bouillot JP, Berger ML, Ben-Ari Y. Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae. Neuroscience. 1984;13:1073–1094
  37. Pérez-Clausell J, Dansher G. Intravesicular localization of zinc in rat telencephalic boutons A histochemical study. Brain Res. 1985;337:91–98
  38. Ribak CE, Navetta MS. An immature mossy fiber innervation of hilar neurons may explain their resistance to kainate-induced cell death in 15 day old rats. Dev. Brain Res. 1994;79:47–62
  39. Sagar HJ, Oxbury JM. Hippocampal neuron loss in temporal lobe epilepsy: Correlation with early childhood convulsions. Ann. Neurol. 1987;22:334–340
  40. Seki T, Arai Y. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J. Neurosci. 1993;1313:2351–2358
  41. Sherwood NM, Timiras PS. A Stereotaxic Atlas of the Developing Rat Brain. Los Angeles: UC Press; 1970;
  42. Sloviter RS. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci. Lett. 1992;137:91–96
  43. Sperber EF, Haas KZ, Stanton PK, Moshé SL. Resistance of the immature brain to seizure-induced synaptic reorganization. Dev. Brain Res. 1991;60:88–93
  44. Sperber EF, Stanton PK, Haas K, Ackermann RF, Moshé SL. Developmental differences in the neurobiology of epileptic brain damage. In:  Engel J,  Wasterlain C,  Cavalheiro EA,  Heinemann U,  Avanzini G editor. Molecular Neurobiology of Epilepsy, Epilepsy Res.. Amsterdam: Elsevier; 1992;p. 67–81 Suppl. 9
  45. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 1989;26:321–330
  46. Tauck DL, Nadler JV. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid treated rats. J. Neurosci. 1985;5:1016–1022
  47. Thompson KW, Holm AM, Wasterlain CG. Loss of hippocampal interneurons in a model of neonatal status epilepticus. Soc. Neurosci. Abstr. 1994;20:1668
  48. Tremblay E, Nitecka L, Berber ML, Ben-Ari Y. Maturation of kainic acid seizure-brain damage syndrome in the rat. I. Clinical, electrographic and metabolic observations. Neuroscience. 1984;13:1051–1072
  49. Wasterlain CG, Sankar R. Excitotoxicity and the developing brain. In:  Avanzini G,  Fariello R,  Heinemann U,  Mutani R editor. Epileptogenic and Excitotoxic Mechanisms. New York: John Libbey & Company Ltd; 1993;p. 135–151
  50. Wasterlain CG, Shirasaka Y. Seizures, brain damage and brain development. Brain Dev. 1994;16:279–295
  51. Zimmer J, Haug FM. Laminar differentiation of the hippocampus, fascia dentata and subiculum in developing rats, observed with the Timm sulphide silver method. J. Comp. Neurol. 1978;179:581–618

PII: S0920-1211(96)00055-1

Epilepsy Research
Volume 26, Issue 1 , Pages 219-231 , December 1996

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