Electrophysiological correlates of seizure sensitivity in the dentate gyrus of epileptic juvenile and adult gerbils

Journal of Neurophysiology

Volumn 76, Issue 4, 1996, Pages 2169-2180

  Buckmaster, Paul S ^a,b   Tam, Edwin ^a   Schwartzkroin, Philip A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN; SOMATOSTATIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPSY; FACILITATION; GERBIL; HIPPOCAMPUS; NERVE CELL INHIBITION; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; SEIZURE;

EID: 0029957576     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.4.2169     Document Type: Article

References (65)

1. ALGER, B. E. AND NICOLL, R. A. GABA-mediated biphasic inhibitory responses in hippocampus. Nature Lond. 281: 315-317, 1979.
2. ANDERSEN, P., BLISS, T. V. P., AND SKREDE, K. K. Unit analysis of hippocampal population spikes. Exp. Brain Res. 13: 208-221, 1971.
3. ANDERSEN, P., DINGLEDINE, R., GJERSTAD, L., LANOMOEN, I. A., AND MOSFELDT LAURSEN, A. Two different responses of hippocampal pyramidal cells to application of gamma-amino butyric acid. J. Physiol. Lond. 305: 279-296, 1980.
4. 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: 2562-2574, 1989.
5. BEN-ARI, Y., CHERUBINI, E., CORRADETTI, R., AND GAIARSA, J.-L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. Lond. 416: 303-325, 1989.
6. BUCKMASTER, P., TAM, E., OWENS, J., AND SCHWARTZKROIN, P. Electrophysiological correlates of seizure-sensitivity in juvenile gerbils (Abstract). Epilepsia 35, Suppl. 8: 3, 1994a.
7. BUCKMASTER, P. S. AND DUDEK, F. E. Inhibition and interneurons in the dentate gyrus of epileptic kainic acid-treated rats (Abstract). Epilepsia 36, Suppl. 4: 40, 1995.
8. BUCKMASTER, P. S., KUNKEL, D. D., ROBBINS, R. J., AND SCHWARTZKROIN, P. A. Somatostatin-immunoreactivity in the hippocampus of mouse, rat, guinea pig, and rabbit. Hippocampus 4: 167-180, 1994b.
9. BUCKMASTER, P. S. AND SCHWARTZKROIN, P. A. Hyperexcitability in the dentate gyrus of the epileptic Mongolian gerbil. Epilepsy Res. 18: 23-28, 1994.
10. B autoreceptors in rat hippocampus. J. Physiol. Lond. 472: 245-265, 1993.
11. 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: 339-355, 1995.
12. FARIAS, P. A., LOW, S. Q., PETERSON, G. M., AND RIBAK, C. E. Morphological evidence for altered synaptic organization and structure in the hippocampal formation of seizure-sensitive gerbils. Hippocampus 1: 229-246, 1992.
13. GROSS-TSUR, V. AND SHINNAR, S. Discontinuing antiepileptic drug treatment. In: The Treatment of Epilepsy: Principles and Practices, edited by E. Wylie. Philadelphia, PA: Lea & Febiger, 1993, p. 858-866.
14. ISOKAWA-AKESSON, M., WILSON, C. L., AND BABB, T. L. Prolonged inhibition in synchronously firing human hippocampal neurons. Epilepsy Res. 3: 236-247, 1989.
15. KAMPHUIS, W., GORTER, J. A., WADMAN, W. J., AND LOPES DA SILVA, F. H. Hippocampal kindling leads to different changes in paired-pulse depression of local evoked field potentials in CA1 area and in fascia dentata. Neurosci. Lett. 141: 101-105, 1992.
16. KAPLAN, H. What triggers seizures in the gerbil, Meriones unguiculatus? Life Sci. 17: 693-698, 1975.
17. KAPLAN, H. AND MIEZEJESKI, C. Development of seizures in the Mongolian gerbil (Meriones unguiculatus). J. Comp. Physiol. Psychol. 81: 267-273, 1972.
18. KAPUR, I., MICHELSON, H. B., BUTERBAUGH, G. G., AND LOTHMAN, E. W. Evidence for a chronic loss of inhibition in the hippocampus after kindling: electrophysiological studies. Epilepsy Res. 4: 90-99, 1989.
19. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419: 119-130, 1987.
20. 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: 388-398, 1988.
21. A receptor-mediated dendritic inhibition in area CA1 of the rat hippocampus. J. Neurophysiol. 66: 1538-1548, 1991.
22. LAMBERT, N. AND GROVER, L. The mechanism of biphasic GABA responses. Science Wash. DC 269: 928-929, 1995.
23. LOSKOTA, W. J. AND LOMAX, P. The Mongolian gerbil (Meriones unguiculatus) as a model for the study of the epilepsies: EEG records of seizures. Eleclroencephalogr. Clin. Neurophysiol. 38: 597-604, 1975.
24. LOSKOTA, W. J., LOMAX, P., AND RICH, S. T. The gerbil as a model for the study of the epilepsies. Epilepsia 15: 109-119, 1974.
25. LUDVIG, N., FARIAS, P. A., AND RIBAK, C. E. An analysis of various environmental and specific sensory stimuli on the seizure activity of the Mongolian gerbil. Epilepsy Res. 8: 30-35, 1991.
26. MAJKOWSKI, J. AND DONADIO, M. Electro-clinical studies of epileptic seizures in Mongolian gerbils. Electroencephalogr. Clin. Neurophysiol. 57: 369-377, 1984.
27. MARGERISON, J. H. AND CORSELLIS, J. A. N. Epilepsy and the temporal lobes: a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89: 499-530, 1966.
28. MARU, E. AND GODDARD, G. V. Alteration in dentate neuronal activities associated with perforant path kindling. Exp. Neurol. 96: 46-60, 1987.
29. MATHERN, G. W., BABB, T. L., PRETORIUS, J. K., AND LEITE, J. P. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J. Neurosci. 15: 3990-4004, 1995.
30. MICHELSON, H. B. AND WONG, R. K. S. Excitatory synaptic responses mediated by GABAA receptors in the hippocampus. Science Wash. DC 253: 1420-1423, 1991.
31. MILGRAM, N. W., MICHAEL, M., CAMMISULI, S., HEAD, E., FERBINTEANU, J., REID, C., MURPHY, M. P., AND RACINE, R. Development of spontaneous seizures over extended electrical kindling. II. Persistence of dentate inhibitory suppression. Brain Res. 670: 112-120, 1995.
32. MILGRAM, N. W., YEARWOOD, T., KHURGEL, M., IVY, G. O., AND RACINE, R. Changes in inhibitory processes in the hippocampus following recurrent seizures induced by systemic administration of kainic acid. Brain Res. 551: 236-246, 1991.
33. MOTT, D. D., BRAGDON, A. C., AND LEWIS, D. V. Phaclofen antagonizes post-tetanic disinhibition in the rat dentate gyrus. Neurosci. Lett. 110: 131-136, 1990.
34. MOTT, D. D., BRAGDON, A. C., LEWIS, D. V., AND WILSON, W. A. Baclofen has a proepileptic effect in the rat dentate gyrus. J. Pharmacol. Exp. Ther. 249: 721-725, 1989.
35. MOURITZEN DAM, A., BAJOREK, J. C., AND LOMAX, P. Hippocampal neuron density and seizures in the Mongolian gerbil. Epilepsia 22: 667-674, 1981.
36. NITSCH, R., LERANTH, C., AND FROTSCHER, M. Most somatostatin-immunoreactive neurons in the rat fascia dentata do not contain the calcium-binding protein parvalbumin. Brain Res. 528: 327-329, 1990.
37. OLIVER, M. W. AND MILLER, J. J. Alterations of inhibitory processes following kindling-induced epilepsy. Exp. Brain Res. 57: 443-447, 1985.
38. PAUL, L. A., FRIED, I., WATANABE, K., FORSYTHE, A. B., AND SCHEIBEL, A. B. Structural correlates of seizure behavior in the Mongolian gerbil. Science Wash. DC 213: 924-926, 1981.
39. PETERSON, G. M. AND RIBAK, C. E. Hippocampus of the seizure-sensitive gerbil is a specific site for anatomical changes in the GABAergic system. J. Comp. Neurol. 261: 405-422, 1987.
40. PETERSON, G. M. AND RIBAK, C. E. Relationship of the hippocampal GABAergic system and genetic epilepsy in the seizure-sensitive gerbil. In: The Hippocampus - New Vistas, edited by V. Chan-Palay and C. Köhler. New York: Liss, 1989, p. 483-497.
41. PETERSON, G. M., RIBAK, C. E., AND OERTEL, W. H. A regional increase in the number of hippocampal GABAergic neurons and terminals in the seizure-sensitive gerbil. Brain Res. 340: 384-389, 1985.
42. RIBAK, C. E., GALL, C. M., AND MODY, I. (Editors). The Dentate Gyrus and Its Role in Seizures. New York: Elsevier, 1992.
43. RIBAK, C. E. AND KHAN, S. U. The effects of knife cuts of hippocampal pathways on epileptic activity in the seizure-sensitive gerbil. Brain Res. 418: 146-151, 1987.
44. RIBAK, C. E. AND PETERSON, G. M. Intragranular mossy fibers in rats and gerbils form synapses with the somata and proximal dendrites of basket cells in the dentate gyrus. Hippocampus 1: 355-364, 1991.
45. SCHWENTKER, V. The gerbil. A new laboratory animal. Ill. Vet. 6: 5-9, 1963.
46. 2+-binding protein parvalbumin. Exp. Brain Res. 85: 137-143, 1991.
47. SETO-OHSHIMA, A., AOKI, E., SEMBA, R., EMSON, P. C., AND HEIZMANN, C. W. Appearance of parvalbumin-specific immunoreactivity in the cerebral cortex and hippocampus of the developing rat and gerbil brain. Histochemistry 94: 579-589, 1990.
48. SIK, A., YLINEN, A., PENTTONEN, M., AND BUZSÁKI, G. Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science Wash. DC 265: 1722-1724, 1994.
49. SLOVITER, R. S. Feedforward and feedback inhibition of hippocampal principal cell activity evoked by perforant path stimulation: GABA-mediated mechanisms that regulate excitability in vivo. Hippocampus 1: 31-40, 1991.
50. 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: 42-60, 1987.
51. A receptors. Science Wash. DC 269: 977-981, 1995.
52. STERIADE, M. AND CONTRERAS, D. Relation between cortical and thalamic cellular events during transition from sleep patterns to paroxysmal activity. J. Neurosci. 15: 623-642, 1995.
53. STRINGER, J. L. AND LOTHMAN, E. W. Maximal dentate gyrus activation: characteristics and alterations after repeated seizures. J. Neurophysiol. 62: 136-143, 1989a.
54. STRINGER, J. L. AND LOTHMAN, E. W. Repetitive seizures cause an increase in paired-pulse inhibition in the dentate gyrus. Neurosci. Lett. 105: 91-95, 1989b.
55. SUTULA, T., CASCINO, G., CAVAZOS, J., PARADA, I., AND RAMIREZ, L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26: 321-330, 1989.
56. THIESSEN, D. D., LINDZEY, G., AND FRIEND, H. C. Spontaneous seizures in the Mongolian gerbil (Meriones unguiculatus). Psychon. Sci. 11: 227-228, 1968.
57. TUFF, L. P., RACINE, R. J., AND ADAMEC, R. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. I. Paired-pulse depression. Brain Res. 277: 79-90, 1983.
58. URUNO, K., O'CONNOR, M. J., AND MASUKAWA, L. M. Effects of bicuculline and baclofen on paired-pulse depression in the dentate gyrus of epileptic patients. Brain Res. 695: 163-172, 1995.
59. VOSKUYL, R. A. AND ALBUS, H. Enhancement of recurrent inhibition by angular bundle kindling is retained in hippocampal slices. Int. J. Neurosci. 36: 153-166, 1987.
60. WANG, X.-J. AND RINZEL, J. Spindle rhythmicity in the reticularis thalami nucleus: synchronization among mutually inhibitory neurons. Neuroscience 53: 899-904, 1993.
61. WEST, M. J., SLOMIANKA, L., AND GUNDERSEN, H. J. G. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231: 482-497, 1991.
62. WHITTINGTON, M. A., TRAUB, R. D., AND JEFFERYS, J. G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature Lond. 373: 612-615, 1995.
63. WONG, R. K. S. AND WATKINS, D. J. Cellular factors influencing GABA response in hippocampal pyramidal cells. J. Neurophysiol. 48: 938-951, 1982.
64. XIE, X. AND SMART, T. G. Properties of GABA-mediated synaptic potentials induced by zinc in adult rat hippocampal pyramidal neurones. J. Physiol. Lond. 460: 503-523, 1993.
65. ZHAO, D. AND LEUNG, L. S. Hippocampal kindling induced paired-pulse depression in the dentate gyrus and paired-pulse facilitation in CA3. Brain Res. 582: 163-167, 1992.