Paleocerebellar electrical stimulation induces the reduction of seizures and the development of absence epilepsy in rats with penicillin-induced epilepsy

Year 2012, , 46 - 51, 17.04.2012

Leonid Godlevsky , Vyacheslav Polyasny Egidius Luijtelaar Antony Coenen

https://doi.org/10.5835/jecm.omu.29.01.012

Abstract

Administration of benzyl penicillin (300,00000 IU/kg, i.p.) in free moving Wistar rats causes the precipitation of spikes and generalized ictal potentials with a life-span of epileptic activity up to 6 hours. Periodic electrical stimulation (ES) of the paleocerebellum (100 Hz, 1 ms, 100-180 A duration of trial 1 s, inter-stimulus interval 3.5-4.0 min) is followed by a significant decrease of the power of epileptic activity, starting at the end of the second hour of stimulation. Moreover, a reduction of the duration of epileptic activity up to 4.0 hours was seen. In the frontal cortex spike-wave discharges (4-5/sec) can be registered starting from 135 to 175 minutes after stimulation. Spike-wave precipitation is followed by a decrease of the amplitude of spikes, by epileptic clonic seizures, by the development of freezing behavior, by tremor, chewing and licking and by other minor signs of absence epilepsy, by vibrissae twitching, by accelerated breathing, head tilting and by eye twitching. Hence, evidence on the absence form of epilepsy precipitation in the course of paleocerebellar-ES-induced suppression of generalized penicillin epilepsy is gained. 

Keywords

Generalized epilepsy, Cerebellar cortex, Spike-wave discharges, Ictal seizures, Electrical stimulation, Rat

References

• Bantli, H., Bloedel, J.R., 1975. Monosynaptic activation of a direct reticulo-spinal pathway by the dentate nucleus. Eur. J. Physioly. 357, 237 242.
• Birioukova, L.M., Loseva, E.V, Ermakova, I.V, Balaban, P.M., 2000. Influence of the substantia nigra allograft on the development of the au diogenic seizures in WAG/Rij rats with mixed fits. In: The WAG/Rij Rat Model of Epilepsy: The Nijmegen-Moscow Research. A Tribute to Five Years Cooperation. 121-127.
• Brighina, F., Daniele, O., Piazza, A., Giglia, G., Fierro, B., 2006. Hemispheric cerebellar rTMS to treat drug-resistant epilepsy: Case reports. Neurosci. Lett. 397, 229-233.
• Buzsaki, G., Laszlovszky, I., Lajtha, A., Vadasz, C., 1990. Spike and wave neocortical patterns in rats: Genetic and aminergic control. Neurosci. 38, 323-333.
• Coenen, A.M.L., Drinkenburg, W.H.I.M., Peeters, B.W.M.M., Vossen, J.M.H., van Luijtelaar, E.L.J.M., 1991. Absence epilepsy and the level of vigilance in rats of the WAG/Rij strain. Neurosci. Biobehav. Rev. 15, 259-263.
• Coenen, A.M.L., Drinkenburg, W.H.I.M., Inoue, M., van Luijtelaar, E.L.J.M., 1992. Genetic models of absence epilepsy, with emphasis on the WAG/Rij strain of rats. Epilepsy Res. 12, 75-86.
• Coenen, A.M.L., Blezer, E.M.H., van Luijtelaar, E.L.J.M., 1995. Effects of the GABA-uptake inhibitor tiagabine on electroencephalogram, spike-wave discharges and behaviour of rats. Epilepsy Res. 21, 89-94.
• Coenen, A.M.L., 2000. Correspondence between absence epilepsy and slow wave sleep. In: The WAG/Rij rat model of epilepsy: The Nijmegen Moscow Research. 27-30.
• Danober, L., Deransart, C., Depaulis, A., Vergnes, M., Marescaux, C., 1998. Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog. Neurobiol. 55, 27- 57.
• Davis, R., 2000. Cerebellar stimulation for central palsy spasticity, function, and seizures. Arc. Med. Res. 31, 290-299.
• Fromm, G.H., 1988. Concepts of the neurophysiologic action of antiepileptic drugs. Am. J. EEG Technol. 28, 185-195.
• Gartside, I.B., 1978. The effects of cerebellectomy on a penicillin epileptogenic focus in the cerebral cortex of the rat. Electroencephalogr. Clin. Neurophysiol. 44, 373-379.
• Gloor, P., 1979. Generalized epilepsy with spike and wave discharges: reinterpretation of its electrographic and clinical manifestations. Epilep sia. 20, 571-588.
• Godlevsky, L.S., van Luijtelaar, E.L.J.M., Shandra, A.A., Coenen, A.M.L., 2002. Cause and effect relations in disease; lessons from epileptic syndromes in animals. Med. Hypotheses. 58, 237-243.
• Godlevsky, L.S., Stepanenko, K.I., Lobasyuk, B.A., Sarahan, E.V., Bobkova, L.M., 2004. The effects of electrical stimulation of the paleocer ebellar cortex on penicillin-induced convulsive activity in rats. Neurosci. Behav. Physiol. 34, 797-802.
• Guyton, A.C., Hall, J.E., 1996. Medical Physiology, ninth ed., New York, Chichester, London, Toronto, W.B.Saunders Company.
• Hablitz, J.J., Rea, G., 1976. Cerebellar nuclear stimulation in generalized penicillin epilepsy. Brain Res. Bull. 1, 599-601.
• Ivanov, S.V., Ward, J.M., Tessarollo, L., McAreavey, D., Sachdev, V., Fananapazir, L., Banks, M.K., Morris, N., Djurickovic, D., Devor-Hen neman, D.E., Wei, M.H., Alvord, G.W., Gao, B., Richardson, J.A., Minna, J.D., Rogawski, M.A., Lerman, M.I., 2004. Cerebellar ataxia, sei zures, premature death, and cardiac abnormalities in mice with targeted disruption of the Cacna2d2 gene. Am. J. Pathol. 165, 1007-1018.
• Kandel, A., Buzsaki, G., 1993. Cerebellar neuronal activity correlates with spike and wave EEG patterns in the rat. Epilepsy Res. 16, 1-9.
• Kahane, P., Depaulis, A., 2010. Deep brain stimulation in epilepsy: What is next? Curr. Opin. Neurol. 23, 177-182.
• Kostopoulos, G., Gloor, P.A., 1982. Mechanism for spike-wave discharges in feline penicillin epilepsy and it's relationship to spindle generation. In: Sleep and Epilepsy. 11-27.
• Kostopoulos, G.K., 2000. Spike-and-wave discharges of absence seizures as a transformation of sleep spindles: The continuing development of a hypothesis. Clin. Neurophysiol. 2, 27-38.
• Kryzhanovsky, G.N., 1986. Central nervous system pathology: A New Approach, New York, Consultant Bureau, Raven Press Publishing Com pany.
• Lason, W., Przewlocka, B., Coenen, A.M.L., Przewolocki, R., van Luijtelaar, E.L.J.M., 1994. Effects of mu and delta opioid receptor agonists and antagonists on absence epilepsy in WAG/Rij rats. Neuropharmacol. 33, 161-166.
• Lason, W., Przewlocka, B., Coenen, A.M.L., Przewlocki, R., Van Luijtelaar, E.L.J.M., 1997. The role of the opioid system in absence epilepsy in rats. In: The WAG/Rij Rat Model of Absence Epilepsy: Ten Years of Research. 182-191.
• Laxer, K.D., Robertson, L.T., Julien, R.M., Dow R.S., 1980. Phenytoin: Relationship between cerebellar function and epileptic discharges. In: Antiepileptic Drugs: Mechanisms of Action. 415-427.
• Lega, B.C., Halpern, C.H., Jaggi, J.L., Baltuch, G.H., 2010. Deep brain stimulation in the treatment of refractory epilepsy: Update on current data and future directions. Neurobiol. Dis. 38, 354-360.
• Lockard, J.S., Ojemann, G.A., Congdon, W.C., Ducharme, L.L., 1979. Cerebellar stimulation in alumina gel monkey model: Inverse relationship between clinical seizures and EEG interictal bursts. Epilepsia. 20, 223-234.
• Lockman, J., Fisher, R.S., 2009. Therapeutic brain stimulation for epilepsy. Clin. Neurol. Neurosur. 27, 1031-1040.
• Marangoz, C., Bağirici, F., 2001. Effects of L-arginine on penicillin-induced epileptiform activity in rats. Jpn. J. Pharmacol. 86, 297-301
• Majkowska-Zwolinska, B., Zurawska, J., 1998. Cerebellar electro stimulation in patients with drug-resistant epilepsy. Neurol. Neurochir. Pol. 2, 181-189.
• Meeren, H.K.M., van Luijtelaar, E.L.J.M., Lopes de Silva, F.H., Berdiev, R.K., Chepurnova, N.E., Chepurnov, S.A., Coenen, A.M.L., 2004. The cortico-thalamic theory for generalized spike- wave discharges. Achievements in Physiological Sciences. 35, 3- 20.
• Morrell, M., 2006. Brain stimulation for epilepsy: can scheduled or responsive neurostimulation stop seizures? Curr. Opin. Neurol. 19, 164 168.
• Paxinos, G., Watson, C., 1998. The rat brain in stereotaxic coordinates, Academic Press Inc., Sydney.
• Peeters, B.W.M.M., van Rijn, C.M., Vossen, J.M.H., Coenen, A.M.L., 1989. Effects of GABA-ergic agents on spontaneous non-convulsive epilepsy, EEG and behaviour, in the WAG/Rij inbred strain of rats. Life Sci. 45, 1171-1176.
• Rubio, C., Custodio, V., Juarez, F., Paz, C., 2004. Stimulation of the superior cerebellar peduncle during the development of amygdaloidal kin dling in rats. Brain Res. 1010, 151-155.
• Shandra, A.A., Godlevsky, L.S., 2005. Pentylenetetrazol-induced kindling as a model of absence and convulsive forms of epilepsy. In: Kindling 6. 49-59.
• Shandra, A.A., Godlevsky, L.S., Mazarati, A.M., Panenko, A.V., Tkachenko, I.V., Chyrkov, Yu, P, 1994. On the mechanisms of antiepileptic factors appearance in the cerebrospinal fluid. Brain Res. Bull. 35, 285-287.
• Shouse, M.N., Siegel, J.M., Wu, M.F., Szymusiak, R., Morrison, A.R., 1989. Mechanisms of seizure suppression during rapid- eye- movement (REM) sleep in cats. Brain Res. 505, 271-282.
• Van Luijtelaar, E.L.J.M., Coenen, A.M.L., 1986. Two types of electro cortical paroxysms in an inbred strain of rats. Neurosci. Lett. 70, 393— 397.
• Velasco, F., Carrillo-Ruiz, J.D., Brito, F., Velasco, M., Velasco, A.L., Marquez, I., Davis, R., 2005. Double-blind, randomized controlled pilot study of bilateral cerebellar stimulation for treatment of intractable motor seizures. Epilepsia. 46, 1071-1081.