Hyperexcitability of entorhinal cortex and hippocampus after application of aminooxyacetic acid (AOAA) to layer III of the rat medial entorhinal cortex in vitro

Journal of Neurophysiology

Volumn 76, Issue 5, 1996, Pages 2986-3001

  Scharfman, Helen E ^a,b  

^a HELEN HAYES HOSPITAL   (United States)

^b College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXAMIC ACID;

ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENTORHINAL CORTEX; EPILEPSY; EPILEPTOGENESIS; HIPPOCAMPUS; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0029861746     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.5.2986     Document Type: Article

References (73)

1. ATILLO, A., SÖDERFELDT, B., KALIMO, H., OLSSON, Y., AND SIESJÖ, B. K. Pathogenesis of brain lesions caused by experimental epilepsy. Acta Neuropathol. 59: 11-24, 1983.
2. BEAL, M. F., SWARTZ, K. J., HYMAN, B. T., STOREY, E., FINN, S. F., AND KOROSHETZ, W. Aminooxyacetic acid results in excitotoxin lesions by a novel indirect mechanism. J. Neurochem. 57: 1068-1073, 1991.
3. BEAR, J. AND LOTHMAN, E. W. An in vitro study of focal epileptogenesis in combined hippocampal-parahippocampal slices. Epilepsy Res. 14: 183-193, 1993.
4. BUZSÁKI, G., PENTTONEN, M., BRAGIN, A., NÁDASDY, Z., AND CHROBAK, J. J. Possible physiological role of the perforant path-CA1 projection. Hippocampus 5: 141-146, 1995.
5. 1H NMR spectroscopic studies. J. Neurochem. 65: 1192-1198, 1995.
6. COLLINS, R. C., TEARSE, R. G., AND LOTHMAN, E. W. Functional anatomy of limbic seizures: focal discharges from medial entorhinal cortex in rat. Brain Res. 280: 25-40, 1983.
7. CONNORS, B. W., GUTNICK, M. J., AND PRINCE, D. A. Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48: 1302-1320, 1982.
8. DANTE ROA, P., TEWS, J. K., AND STONE, W. E. A neurochemical study of thiosemicarbazide seizures and their inhibition by amino-oxyacetic acid. Biochem. Pharmacol. 13: 477-487, 1964.
9. DASHEIFF, R. M. AND MCNAMARA, J. O. Electrolytic entorhinal lesions cause seizures. Brain Res. 231: 444-450, 1982.
10. DA VANSO, J. P., GREIG, M. E., AND CRONIN, M. A. Anticonvulsant properties of amino-oxyacetic acid. Am. J. Physiol. 201: 833-837, 1961.
11. DAVIES, C. H., DAVIES, S. N., AND COLLINGRIDGE, G. L. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in hippocampus. J. Physiol. Lond. 424: 513-531, 1990.
12. B receptor feedback on GABA release. J. Physiol. Lond. 412: 513-541, 1989.
13. DESMOND, N. L., SCOTT, C. A., JANE, J. A., AND LEVY, W. B. Ultrastructural identification of entorhinal cortical synapses in CA1 stratum lacunosum-moleculare of the rat. Hippocampus 4: 594-600, 1994.
14. DEUTSCH, C., SPENCER, S., ROBBINS, R., CICCHETTI, D., AND SPENCER, D. Interictal spikes and hippocampal somatostatin levels in temporal lobe epilepsy. Epilepsia 32: 174-178, 1991.
15. DU, F., EID, T., LOTHMAN, E. W., KÖHLER, C., AND SCHWARCZ, R. Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J. Neurosci. 15: 6301-6313, 1995.
16. DU, F. AND SCHWARCZ, R. Aminooxyacetic acid causes selective neuronal loss in layer III of the rat medial entorhinal cortex. Neurosci. Lett. 147: 185-188, 1992.
17. DU, F., WHETSELL, W. O., ABOU-KHALIL, B., BLUMENKOPF, B., LOTHMAN, E. W., AND SCHWARCZ, R. Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy. Epilepsy Res. 16: 223-233, 1993.
18. EID, T., DU, F., AND SCHWARCZ, R. Differential neuronal vulnerability to aminooxyacetic acid and quinolinic acid in the rat parahippocampal region. Neuroscience 68: 645-656, 1995.
19. EMPSON, R. M. AND HEINEMANN, U. Perforant path connections to area CA1 are predominantly inhibitory in the rat hippocampal-entorhinal cortex combined slice preparation. Hippocampus 5: 104-107, 1995.
20. FITZPATRICK, S. M., COOPER, A. J. L., AND DUFFY, T. E. Use of beta methylene-D,L-aspartate to assess the role of aspartate aminotransferase in cerebral oxidative metabolism. J. Neurochem. 41: 1370-1383, 1983.
21. GANONG, A. H., LANTHORN, T. H., AND COTMAN, C. W. Kynurenic acid inhibits synaptic and acidic amino acid-induced responses in rat hippocampus and spinal cord. Brain Res. 273: 170-174, 1983.
22. GOLDRING, S., EDWARDS, I., HARDING, G. W., AND BERNARDO, K. L. Results of anterior temporal lobectomy that spares the amygdala in patients with complex partial seizures. J. Neurosurg. 77: 185-193, 1992.
23. HARVEY, S. C. Hypnotics and sedatives. In: The Pharmacological Basis of Therapeutics, edited by A. G. Gilman, L. S. Goodman, T. W., Rall and R. Murad. New York: Macmillan, 1985, p. 339-371.
24. HEINEMANN, U., BECK, H., DREIER, J. P., FICKER, E., STABEL, J., AND ZHANG, C. L. The dentate gyrus as a regulated gate for the propagation of epileptiform activity. In: The Dentate Gyrus and Its Role In Seizures, edited by C. E. Ribak, C. M. Gall, and I. Mody. Amsterdam: Elsevier, 1992, p. 273-280.
25. HERKENHAM, M. The connection of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J. Comp. Neurol. 177: 589-610, 1978.
26. HJORTH-SIMONSEN, A. AND JEUNE, B. Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144: 215-232, 1972.
27. HOWE, J. R., SUTOR, B., AND ZIEGLGANSBERGER, W. Baclofen reduces postsynaptic potentials of rat cortical neurons by an action other than its hyperpolarizing action. J. Physiol. Lond. 384: 539-570, 1987.
28. JONES, K. AND BAUGHMAN, R. W. NMDA and non NMDA receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex. J. Neurosci. 8: 3522-3534, 1988.
29. JONES, R. S. G. Complex synaptic responses of entorhinal cortical cells in the rat to subicular stimulation in vitro: demonstration of an NMDA receptor-mediated component. Neurosci. Lett. 81: 209-214, 1987.
30. JONES, R. S. G. AND HEINEMANN, U. Synaptic and intrinsic responses of medial entorhinal cortical cells in normal and magnesium-free medium in vitro. J. Neurophysiol. 59: 1476-1496, 1988.
31. JONES, R. S. G. AND LAMBERT, J. D. C. Synchronous discharges in the rat entorhinal cortex in vitro: site of initiation and the role of excitatory amino acid receptors. Neuroscience 34: 657-670, 1990a.
32. JONES, R. S. G. AND LAMBERT, J. D. C. The role of excitatory amino acid receptors in the propagation of epileptiform discharges from the entorhinal cortex to the dentate gyrus in vitro. Exp. Brain Res. 80: 310-322, 1990b.
33. A-mediated IPSP regulates facilitation of NMDA-mediated responses to burst stimulation of afferent fibers in piriform cortex. J Neurosci. 16: 307-312, 1995.
34. KAUPPINEN, R. A., SIHRA, T. S., AND NICHOLLS, D. Aminooxyacetic acid inhibits the malate-aspartate shuttle in isolated nerve terminals and prevents the mitochondria from utilizing glycolytic substrates. Biochim. Biophys. Acta 930: 173-178, 1987.
35. KIM, J. H., GUIMARAES, P. O., SHEN, M. Y., MASUKAWA, L. M., AND SPENCER, D. D. Hippocampal neuronal density in temporal lobe epilepsy with and without gliomas. Acta Neuropathol. 80: 41-45, 1990.
36. KÖHLER, C. Intrinsic projections of the retrohippocampal region in the rat brain. II. The medial entorhinal area. J. Comp. Neurol. 246: 149-169, 1986.
37. LEUNG, L.-W. S. Simulation of perforant path evoked field and intracellular potentials in hippocampal CA1 area. Hippocampus 5: 129-136, 1995.
38. LEVESQUE, M. F., NAKASATO, N., VINTERS, H. V., AND BABB, T. L. Surgical treatment of limbic epilepsy associated with extrahippocampal lesions: the problem of dual pathology. J. Neurosurg. 75: 364-370, 1991.
39. LEVY, W. B., COLBERT, C. M., AND DESMOND, N. L. Another network model bites the dust: entorhinal inputs are no more than weakly excitatory in the hippocampal CA1 region. Hippocampus 5: 137-140, 1995.
40. LÖSCHER, W. AND FREY, H. H. Aminooxyacetic acid: correlation between biochemical effects, anticonvulsant action, and toxicity in mice. Biochem. Pharmacol. 27: 103-108, 1978.
41. LOTHMAN, E. W., BERTRAM, E. H., BEKENSTEIN, J. W., AND PERLIN, J. B. Self-sustaining limbic status epilepticus induced by continuous hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res. 3: 107-119, 1989.
42. LOTHMAN, E. W., BERTRAM, E. H., AND STRINGER, J. L. Functional anatomy of hippocampal seizures. Prog. Neurobiol. 37: 1-82, 1991.
43. o in the adult rat entorhinal cortex maintained in vitro. Neurosci. Lett. 185: 155-158, 1995.
44. LUHMANN, H. J. AND PRINCE, D. A. Control of NMDA receptor-mediated activity by GABAergic mechanisms in mature and developing rat neocortex. Dev. Brain Res. 54: 287-290, 1990.
45. MCCORMICK, D. A., CONNORS, B. W., LIGHTHALL, J. W., AND PRINCE, D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54: 782-806, 1985.
46. MCMASTER, O. G., DU, F., FRENCH, E. D., AND SCHWARCZ, R. Focal injection of aminooxyacetic acid produces seizures and lesions in rat hippocampus: evidence for mediation by NMDA receptors. Exp. Neurol. 113: 378-385, 1991.
47. METHERATE, R. AND ASHE, J. H. Facilitation of an NMDA receptor-mediated EPSP by paired-pulse stimulation in rat neocortex via depression of GABAergic IPSPs. J. Physiol. Lond. 481: 331-348, 1994.
48. MORIN, G. AND GASTAUT, H. Normal and Pathological Anatomical Problems Raised by Epileptic Discharges. Brussels: Acta Medica Belgica, 1954.
49. B autoreceptors mediate activity-dependent disinhibition and enhance signal transmission in the dentate gyrus. J. Neurophysiol. 69: 674-691, 1993.
50. PALAIPLOGOS, G., HERTZ, L., AND SCHOUSBOE, A. Evidence that aspartate aminotransferase activity and ketodicarboxylate carrier function are essential for the biosynthesis of transmitter glutamate. J. Neurochem. 51: 317-320, 1988.
51. PARÉ, D. AND LLINÁS, R. Intracellular study of direct entorhinal inputs to field CA1 in the isolated guinea pig brain in vitro. Hippocampus 5: 115-119, 1995.
52. PAXINOS, G. AND WATSON, C. The Rat Brain in Stereotaxic Coordinates. London: Academic, 1986.
53. RUTH, R. E., COLLIER, T. J., AND ROUTTENBERG, A. Topography between the entorhinal cortex and the dentate septotemporal axis in rats. I. Medial and intermediate entorhinal projecting cells. J. Comp. Neurol. 209: 69-78, 1982.
54. RUTH, R. E., COLLIER, T. J., AND ROUTTENBERG, A. Topographical relationship between the entorhinal cortex and the septotemporal axis of the dentate gyrus in rats. II. Cells projecting from lateral entorhinal subdivision. J Comp. Neurol. 270: 506-516, 1988.
55. SCHARFMAN, H. E. Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J. Neurophysiol. 74: 179-194, 1995.
56. SOLTESZ, I. AND JONES, R. S. G. The direct perforant path input to CA1: excitatory or inhibitory? Hippocampus 5: 101-103, 1995.
57. SPECIALE, C., WU, H., GRAMSBERGEN, J. B. P., TURSKI, W. A., UNGERSTEDT, U., AND SCHWARCZ, R. Determination of extracellular kynurenic acid in the striatum of unanesthetized rats: effect of aminooxyacetic acid. Neurosci. Lett. 116: 198-203, 1990.
58. SPENCER, D. D. Classifying the epilepsies by substrate. Clin. Neurosci. 2: 104-109, 1994.
59. SPENCER, S. S. AND SPENCER, D. D. Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia 35: 721-727, 1994.
60. STEWARD, O. Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. Comp. Neurol. 167: 285-314, 1976.
61. STEWARD, O. AND SCOVILLE, S. A. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169: 347-370, 1976.
62. STONE, T. W., BURTON, N. R., AND SMITH, D. A. Electrophysiology of quinolinic acid and other kynurenines and their potential roles in the CNS. In: Quinolinic Acid and the Kynurenines, edited by T. W. Stone. Boca Raton, FL: CRC, 1989, p. 114-148.
63. SUTOR, B. AND HABLITZ, J. J. EPSPs in rat neocortical neurons in vitro. II. Involvement of N-methyl-D-aspartate receptors in the generation of EPSPs. J. Neurophysiol. 61: 621-634, 1989.
64. TAPIA, R., PEREZ DE LA MORA, M., AND MASSIEU, G. H. Correlative changes of pyridoxal kinase pyridoxal-5′-phosphate and glutamate decarboxylase in brain during drug-induced convulsions. Ann. NY Acad. Sci. 166: 257-266, 1969.
65. THOMSON, A. A magnesium-sensitive post-synaptic potential in rat cerebral cortex resembles neuronal responses to N-methylaspartate. J. Physiol. Lond. 370: 531-549, 1986.
66. TURSKI, W. A., GRAMSBERGEN, J. B. P., TRAITLER, H., AND SCHWARCZ, R. Rat brain slices produce and liberate kynurenic acid upon exposure to L-kynurenine. J. Neurochem. 52: 1629-1636, 1989.
67. WALTHER, H., LAMBERT, J. D. C., JONES, R. S. G., HEINEMANN, U., AND HAMON, B. Epileptiform activity in combined slices of the hippocampus, subiculum and entorhinal cortex during perfusion with low magnesium medium. Neurosci. Lett. 69: 156-161, 1986.
68. WITTER, M. P., GRIFFOEN, A. W., JORRITSMA-BYHAM, B., AND KRIJNEN, J. L. M. Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci. Lett. 85: 193-198, 1988.
69. WITTER, M. P., GROENEWEGEN, H. J., LOPES DA SILVA, F. H., AND LOHMAN, A. H. M. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33: 161-253, 1989a.
70. WITTER, M. P., VAN HOESEN, G. W., AND AMARAL, D. G. Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J. Neurosci. 9: 216-228, 1989b.
71. WOOD, J. D. AND PEESKER, S. J. The role of GABA metabolism in the convulsant and anticonvulsant actions of aminooxyacetic acid. J. Neurochem. 20: 379-387, 1973.
72. WOUTERLOOD, F. G., SALDANA, E., AND WITTER, M. P. Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 199: 495-412, 1990.
73. YECKEL, M. F. AND BERGER, T. W. Monosynaptic excitation of hippocampal CA1 pyramidal cells by afferents from the entorhinal cortex. Hippocampus 5: 108-114, 1995.