Abstract
We observed in this study that transient periodic stimuli in response to high potassium (40 mM, 5 min at 40-min intervals, 13–15 stimuli) perfusion in the ventral hippocampus of rats led to the appearance of a kindling-like phenomenon. In this kindling-like phenomenon, we confirmed the augmentation of glutamate release and the prolongation of spike discharge. Changes in the extracellular glutamate levels before and after the stimuli were monitored by the application of in vivo microdialysis combined with on-line enzyme fluorometric detection of glutamate. This kindling-like phenomenon was not observed when microdialysis was carried out using a Ca++-free medium. The augmentation of glutamate release and the prolongation of spike discharge with epileptic convulsions are completely Ca++ dependent. These data show that repeated short-term increases in extracellular glutamate levels results in the enhancement of excitatory neuronal systems, causing an excessive propagation of seizure activity and culminating in secondary generalized seizures.
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References
Bading H, Ginty DD, Greenberg ME (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260:181–186
Croucher MJ, Bradford HF (1989) Kindling of full limbic seizures by repeated microinjections of excitatory amino acids into the rat amygdala. Brain Res 501:58–65
During MJ, Spencer DD (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341:1607–1610
Fritz LC, Gardner-Medwin AR (1976) The effect of synaptic activation on the extracellular potassium concentration in the hippocampal dentate area, in vitro. Brain Res 112:183–187
Ghosh A, Greenberg ME (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268:239–247
Goddard GV, Mclntyre DC, Leech CAK (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25:295–330
Graham LT, Aprison MH (1966) Fluorometric determination of aspartate, glutamate and gamma-aminobutyrate in nerve tissue using enzymatic methods. Anal Biochem 15:487–497
Herron CE, Lester RA, Coan EJ, Collingridge GL (1986) Frequency-dependent involvement of NMDA receptors in the hippocampus: a novel synaptic mechanism. Nature 322:265–268
Jarvie PA, Logan TC, Geula C, Slevin JT (1990) Entorhinal kindling permanently enhances Ca++-dependent l-glutamate release in regio inferior of rat hippocampus. Brain Res 508: 188–193
Lothman EW, Beneath JP, Peril JB (1987) Alterations in neurotransmitter amino acids in hippocampal kindled seizures. Epilepsy Res 1:313–320
Maru E, Goddard GV (1987) Alteration in dentate neuronal activities associated with perforant path kindling. Exp Neurol 96:19–32
Matsuda K, Ueda Y, Haruta A, Tono T, Komune S (1998) High potassium-induced glutamate release in the cochlea: in vivo microdialysis study combined with on-line enzyme fluorometric detection of glutamate. Brain Res 794:343–346
Minamoto Y, Itano T, Tokuda M, Matsui H, Janjua NA, Hosokawa K, Okada Y, Murakami TH, Negi T, Hatase O (1992) In vivo microdialysis of amino acid neurotransmitters in the hippocampus in amygdaloid kindled rat. Brain Res 573:345–348
Mori N, Wada JA (1987) Bidirectional transfer between kindling induced by excitatory amino acids and electrical stimulation. Brain Res 425:45–48
Morimoto K, Katayama K, Inoue K, Sato K (1991) Effects of competitive and noncompetitive NMDA receptor antagonists on kindling and LTP. Pharmacol Biochem Behav 40:893–899
Nakahara D, Ozaki N, Miura Y, Miura H, Nagatsu T (1989) Increased dopamine and serotonin metabolism in rat nucleus accumbens produced by intracranial self-stimulation of medial forebrain bundle as measured by in vivo microdialysis. Brain Res 495:178–181
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, New York
Perez-Pinzon MA, Tao L, Nicholson C (1995) Extracellular potassium, volume fraction and tortuosity in rat hippocampal CA1, CA3 and cortical slices during ischemia. J Neurochem 74: 565–573
Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281–294
Semyanov A, Godukhin O (1997) Kindling-like state in rat hippocampal CA1 slices induced by the repeated short-term extracellular K+ increases: the role of L-type Ca2+-channels. Neurosci Lett 223:177–180
Semyanov A, Kalemenev SV, Godukhin O (1997) Kindling-like state occurring on periodic increases in the extracellular K+ concentration in field CA1 in rat hippocampal slices. Neurosci Behav Physiol 28:504–512
Somjen GG, Giacchino LJ (1985) Potassium and calcium concentrations in interstitial fluid of hippocampal formation during paroxysmal responses. J Neurophysiol 53:1098–1108
Ueda Y, Tsuru N (1994) Bilateral seizure-related changes of extra-cellular glutamate concentration in hippocampi during development of amygdaloid kindling. Epilepsy Res 18:85–88
Ueda Y, Tsuru N (1995) Simultaneous monitoring of the seizure-related changes in extracellular glutamate and γ-aminobutyric acid concentration in bilateral hippocampi following development of amygdaloid kindling. Epilepsy Res 20:213–219
Zhang WQ, Hudson PM, Sobotka TJ, Hong JS, Tilson HA (1991) Extracellular concentrations of amino acid transmitters in ventral hippocampus during and after the development of kindling. Brain Res 540:315–318
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Published online: 27 July 2000
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Ueda, Y., Doi, T., Tokumaru, J. et al. Kindling phenomena induced by the repeated short-term high potassium stimuli in the ventral hippocampus of rats: on-line monitoring of extracellular glutamate overflow. Exp Brain Res 135, 199–203 (2000). https://doi.org/10.1007/s002210000509
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DOI: https://doi.org/10.1007/s002210000509