Hippocampal High-Frequency Stimulation Inhibites the Progression of Rapid Kindling-Induced Seizure in Rats — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Hippocampal High-Frequency Stimulation Inhibites the Progression of Rapid Kindling-Induced Seizure in Rats
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
,
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
,
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
,
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
,
Laboratory of Biomedical Technology, Department of Electronics, Buenos Aires Faculty, National Technological University (UTN), Buenos Aires, Argentina.
,
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
,
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
,
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
,
Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
1 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
2 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
3 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
4 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
5 Laboratory of Biomedical Technology, Department of Electronics, Buenos Aires Faculty, National Technological University (UTN), Buenos Aires, Argentina.
6 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
7 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina;
8 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
9 Center of Clinical and Experimental Neuroscience, Epilepsy, Cognition and Behavior, Institute of Cellular Biology and Neuroscience “Prof. E. De Robertis” (IBCN)-National Council for Scientific and Technical Research (CONICET), School of Medicine, University of Buenos Aires, Buenos Aires, Argentina
Epilepsy is one of the most common serious neurological disorders. Pharmacoresistant epilepsy patients are poorly controlled or their seizures are refractory to drug treatment. Resective surgery is frequently a promising therapy in this population, however, not all the patients meet the eligibility criteria for the surgical treatment. Deep brain stimulation has been investigated in clinical studies and animal studies as an alternative treatment, but the optimal stimulation pa rameters remain an issue. The present study was designed to investigate the effect of unilateral high - frequency stimula tion (HFS) of hippocampus on seizure development by using the hippocampal rapid kindling method (hRK) in rats, and compared th e results with those of low-frequency stimulation previously published by our group. We used male Wistar rats implanted with electrodes in the ventral hippocampus. All rats underwent hRK (biphasic square wave pulses, 20 Hz for 10 seconds) during three consecutive days (twelve stimulations per day). The control group (hRK; n = 7) received only RK stimulus, while the treated group (HFS-hRK; n = 9) received also HFS (biphasic square wave pulses, 130 Hz for 30 seconds) immediately before the RK stimulus, during three consecutive days. At the end of behavioral testing 78% (p < 0.01) of the animals receiving HFS treatment were still not fully kindled staying in stages 0 - III (p < 0.01). HFS group needed a higher number of stimulations to achieve stage III (p < 0.05) with respect to control group. How ever, no significant differences in the cumulative daily afterdischarge duration were observed. HFS did not present sig nificant differences compared with LFS in any of studied parameters. Th e findings suggest that unilateral HFS applied on hippocampus effectively inhibited the epileptogenic process induced by hippocampal rapid kindling. According to the comparative results about hippocampal rapid kindled animals stimulated with HFS and LFS (5 Hz), we found no conclusive information on which treatment is most efficient.
T. Dua, H. M. de Boer, L. L. Prilipko and S. Saxena, “Epilepsy Care in the World: Results of an ILAE/IBE/ WHO Global Campaign against Epilepsy Survey,” Epilepsia, Vol. 47, No. 7, 2006, pp. 1225-1231. doi:10.1111/j.1528-1167.2006.00595.x
P. Kwan, A. Arzimanoglou, A. T. Berg, M. J. Brodie, W. A. Hauser, G. Mathern, S. L. Moshé, E. Perucca, S. Wiebe and J. French, “Definition of Drug Resistant Epilepsy: Consensus Proposal by the Ad Hoc Task Force of the ILAE Commission on Therapeutic Strategies,” Epilepsia, Vol. 51, No. 6, 2010, pp. 1069-1077. doi:10.1111/j.1528-1167.2009.02397.x
I. S. Cooper, I. Amin, M. Riklan, J. M. Waltz and T. P. Poon, “Chronic Cerebellar Stimulation in Epilepsy. Clinical and Anatomical Studies,” Archives of Neurology, Vol. 33, No. 8, 1976, pp. 559-570. doi:10.1001/archneur.1976.00500080037006
A. R. Upton, I. S. Cooper, M. Springman and I. Amin, “Suppression of Seizures and Psychosis of Limbic System Origin by Chronic Stimulation of Anterior Nucleus of the Thalamus,” International Journal of Neurology, Vol. 19-20, 1985-1986, pp. 223-230.
F. Velasco, M. Velasco, C. Ogarrio and G. Fanghanel, “Electrical Stimulation of the Centromedian Thalamic Nucleus in the Treatment of Convulsive Seizures: A Preliminary Report,” Epilepsia, Vol. 28, No. 4, 1987, pp. 421-430. doi:10.1111/j.1528-1157.1987.tb03668.x
M. Velasco, F, Velasco, A. L. Velasco, F. Jiménez, F. Brito and I. Márquez, “Acute and Chronic Electrical Stimulation of the Centromedian Thalamic Nucleus: Modulation of Reticulo-Cortical Systems and Predictor Factors for Generalized Seizure Control,” Archives of Medical Research, Vol. 31, No. 3, 2000, pp. 304-315. doi:10.1016/S0188-4409(00)00085-0
M. Velasco, F. Velasco and A. L. Velasco, “Centromedian-Thalamic and Hippocampal Electrical Stimulation for the Control of Intractable Epileptic Seizures,” Journal of Clinical Neurophysiology, Vol. 18, No. 6, 2001, pp. 495-513. doi:10.1097/00004691-200111000-00001
A. Schulze-Bonhage, “Deep Brain Stimulation: A New Approach to the Treatment of Epileps,” Deutsches Ärzteblatt International, Vol. 106, No. 24, 2009, pp. 407-412.
B. C. Jobst, “Brain Stimulation for Surgical Epilepsy,” Epilepsy Research, Vol. 89, No. 1, 2010, pp. 154-161. doi:10.1016/j.eplepsyres.2009.08.017
SANTE Study Group, “Electrical Stimulation of the Anterior Nucleus of Thalamus for Treatment of Refractory Epilepsy,” Epilepsia, Vol. 51, No. 5, 2010, pp. 899-908. doi:10.1111/j.1528-1167.2010.02536.x
T. Tykocki, T. Mandat, A. Kornakiewicz, H. Koziara and P. Nauman, “Deep Brain Stimulation for Refractory Epilepsy,” Archives of Medical Science, Vol. 8, No. 5, 2012, pp. 805-816. doi:10.5114/aoms.2012.31135
G. V. Goddard, D. C. McIntyre and C. K. Leech, “A Permanent Change in Brain Function Resulting from Daily Electrical Stimulation,” Experimental Neurology, Vol. 25, No. 3, 1969, pp. 295-330. doi:10.1016/0014-4886(69)90128-9
G. V. Goddard, “The Kindling Model of Epilepsy,” Trends in Neurosciences, Vol. 6, 1983, pp. 275-279. doi:10.1016/0166-2236(83)90118-2
J. O. McNamara, D. W. Bonhaus and C. Shin, “The Kindling Model of Epilepsy,” In: P. A. Schwartzkroin, Ed., Epilepsy: Models, Mechanisms, and Concepts, Cambridge University Press, Cambridge, 1993, pp. 27-47. doi:10.1017/CBO9780511663314.003
A. Mazarati, D. Shin, S. Auvin, R. Caplan and R. Sankar, “Kindling Epileptogenesis in Immature Rats Leads to Persistant Depressive Bahavior,” Epilepsy and Behavior, Vol. 10, No. 3, 2007, pp. 377-383. doi:10.1016/j.yebeh.2007.02.001
E. W. Lothman, J. M. Hatlelid, C. F. Zorumski, J. A. Conry, P. F. Moon and J. B. Perlin, “Kindling with Rapidly Recurring Hippocampal Seizures,” Brain Research, Vol. 360, No. 1-2, 1985, pp. 83-91. doi:10.1016/0006-8993(85)91223-5
E. W. Lothman and J. M. Williamson, “Rapid Kindling with Recurrent Hippocampal Seizures,” Epilepsy Research, Vol. 14, No. 3, 1993, pp. 209-220. doi:10.1016/0920-1211(93)90045-9
E. W. Lothman and J. M. Williamson, “Closely Spaced Recurrent Hippocampal Seizures Elicit Two Types of Heightened Epileptogenesis: A Rapidly Developing, Transient Kindling and a Slowly Developing, Enduring Kindling,” Brain Research, Vol. 649, No. 1-2, 1994, pp. 71-84. doi:10.1016/0006-8993(94)91050-2
J. H. Goodman, R. E. Berger and T. K Tcheng, “Preemptive Low-Frequency Stimulation Decreases the Incidence of Amygdala-Kindled Seizures,” Epilepsia, Vol. 46, No. 1, 2005, pp. 1-7. doi:10.1111/j.0013-9580.2005.03804.x
L. X. Yang, C. L. Jin, Z. B. Zhu-Ge, S. Wang, E. Q. Wei, I. C. Bruce and Z. Chen, “Unilateral Low-Frequency Stimulation of Central Piriform Cortex Delays Seizure Development Induced by Amygdaloid Kindling in Rats,” Neuroscience, Vol. 138, No. 4, 2006, pp. 1089-1096. doi:10.1016/j.neuroscience.2005.12.006
M. Mohammad-Zadeh, J. Mirnajafi-Zadeh, Y. Fathollahi, M. Javan, P. Ghorbani, M. Sadegh and S. M. Noorbakhsh, “Effect of Low Frequency Stimulation of Perforant Path on Kindling Rate and Synaptic Transmission in the Dentate Gyrus during Kindling Acquisition in Rats,” Epilepsy Research, Vol. 75, No. 2-3, 2007, pp. 154-161. doi:10.1016/j.eplepsyres.2007.05.003
S. H. Zhang, H. L. Sun, Q. Fang, K. Zhong, D. C. Wu, S. Wang and Z. Chen, “Low-Frequency Stimulation of the Hippocampal CA3 Subfield Is Anti-Epileptogenic and Anti-Ictogenic in Rat Amygdaloid Kindling Model of Epilepsy,” Neuroscience Letters, Vol. 455, No. 1, 2009, pp. 51-55. doi:10.1016/j.neulet.2009.03.041
M. Sadegh, J. Mirnajafi-Zadeh and V. Sheibani, “Serine/ Threonine Protein Phosphatases Have No Role in the Inhibitory Effects of Low-Frequency Stimulation in Perforant Path Kindling Acquisition in Rats,” Neuroscience Letters, Vol. 451, No. 3, 2009, pp. 266-269. doi:10.1016/j.neulet.2009.01.001
M. Cuellar-Herrera, L. Neri-Bazan and L. L. Rocha, “Behavioral Effects of High Frequency Electrical Stimulation of the Hippocampus on Electrical Kindling in Rats,” Epilepsy Research, Vol. 72, No. 1, 2006, pp. 10-17. doi:10.1016/j.eplepsyres.2006.07.002
T. Wyckhuys, T. De Smedt, P. Claeys, R. Raedt, L. Waterschoot, K. Vonck, C. Van den Broecke, C. Mabilde, L. Leybaert, W. Wadman and P. Boon, “High Frequency Deep Brain Stimulation in the Hippocampus Modifies Seizure Characteristics in Kindled Rats,” Epilepsia, Vol. 48, No. 8, 2007, pp. 1543-50. doi:10.1111/j.1528-1167.2007.01038.x
Q. Zhang, Z. C. Wu, J. T. Yu, N. N. Yu, X. L. Zhong and L. Tan, “Mode-Dependent Effect of High-Frequency Electrical Stimulation of the Anterior Thalamic Nucleus on Amygdala-Kindled Seizures in Rats,” Neuroscience, Vol. 217, 2012, pp. 113-122. doi:10.1016/j.neuroscience.2012.05.009
T. Wyckhuys, R. Raedt, K. Vonck, W. Wadman and P. Boon, “Comparison of Hippocampal DBS with High (130 Hz) and Low (5 Hz) Frequency on Afterdischarges in Kindled Rats,” Epilepsy Research, Vol. 88, No. 2-3, 2010, pp. 239-246. doi:10.1016/j.eplepsyres.2009.11.014
L. Toibaro, M. Pereyra, J. Pastorino, A. Smigliani, F. Ocariz, G. Ortmann, M. M. Galardi, M. B. Gori and S. Kochen, “Effect of Unilateral Low-Frequency Stimulation of Hippocampus on Rapid Kindling-Induced Seizure Development in Rats,” Neuroscience and Medicine, Vol. 3, No. 2, 2012, pp. 174-180. doi:10.4236/nm.2012.32022
D. King, S. S. Spencer, G. McCarthy, M. Luby and D. D. Spencer, “Bilateral Hippocampal Atrophy in Medial Temporal-Lobe Epilepsy,” Epilepsia, Vol. 36, No. 9, 1995, pp. 905-910. doi:10.1111/j.1528-1157.1995.tb01634.x
T. H. Swanson, “The Pathophysiology of Human Mesial Temporal Lobe Epilepsy,” Journal of Clinical Neurophysiology, Vol. 12, No. 1, 1995, pp. 2-22. doi:10.1097/00004691-199501000-00001
S. S. Spencer, “Neural Networks in Human Epilepsy: Evidence of and Implications for Treatment,” Epilepsia, Vol. 43, No. 3, 2002, pp. 219-227. doi:10.1046/j.1528-1157.2002.26901.x
G. Paxinos and C. Watson, “The Rat Brain in Stereotaxic Coordinates,” 4th Edition, Academic Press, San Diego, 1998.
K. Vonck, P. Boon, E. Achten, J. De Reuck and J. Caemaert, “Long-Term Amygdalohippocampal Stimulation for refractory Temporal Lobe Epilepsy,” Annals of Neurology, Vol. 52, No. 5, 2002, pp. 556-565. doi:10.1002/ana.10323
R. J. Racine, “Modification of Seizure Activity by Electrical Stimulation: I. Afterdischarge Threshold and II. Motor Seizure,” Electroencephalography and Clinical Neurophysiology, Vol. 32, No. 3, 1972, pp. 269-294. doi:10.1016/0013-4694(72)90176-9
D. C. McIntyre, M. O. Poulter and K. Gilby, “Kindling: Some Old and Some New,” Epilepsy Research, Vol. 50, No. 1-2, 2002, pp. 79-92. doi:10.1016/S0920-1211(02)00071-2
M. Sato, R. J. Racine and D. C. McIntyre, “Kindling: Basic Mechanisms and Clinic Validity,” Electroencephalography and Clinical Neurophysiology, Vol. 76, No. 5, 1990, pp. 459-472. doi:10.1016/0013-4694(90)90099-6
F. Velasco, M. Velasco, F. Jiménez, A. L. Velasco, F. Brito, M. Rise and J. D. Carrillo-Ruiz, “Predictors in the Treatment of Difficult-to-Control Seizures by Electrical Stimulation of the Centromedian Thalamic Nucleus,” Neurosurgery, Vol. 47, No. 2, 2000, pp. 295-305. doi:10.1097/00006123-200008000-00007
A. L. Velasco, M. Velasco, F. Velasco, D. Menes, L. Rocha, M. Briones and I. Márquez, “Subacute and Chronic Electrical Stimulation of the Hippocampus on Intractable Temporal Lobe Seizures: Preliminary Report,” Archives of Medical Research, Vol. 31, No. 3, 2000, pp. 316-328. doi:10.1016/S0188-4409(00)00064-3
K. Vonck, P. Boon, P. Claeys, S. Dedeurwaerdere, R. Achten and D. Van Roost, “Long-Term Deep Brain Stimulation for Refractory Temporal Lobe Epilepsy,” Epilepsia, Vol. 46, Suppl. 5, 2005, pp. 98-99. doi:10.1111/j.1528-1167.2005.01016.x
L. Vercueil, A. Benazzouz, C. Deransart, K. Bressand, C. Marescaux, A. Depaulis and A. L. Benabid, “High-Frequency Stimulation of the Subthalamic Nucleus Suppresses Absence Seizures in the Rat: Comparison with Neurotoxic Lesions,” Epilepsy Research, Vol. 31, No. 1, 1998, pp. 39-46. doi:10.1016/S0920-1211(98)00011-4
A. L. Benabid, “Deep Brain Stimulation for Parkinson’s Disease,” Current Opinion in Neurobiology, Vol. 13, No. 6, 2003, pp. 696-706. doi:10.1016/j.conb.2003.11.001
B. C. Albensi, G. Ata, E. Schmidt, J. D. Waterman and D. Janigro, “Activation of Long-Term Synaptic Plasticity Causes Suppression of Epileptiform Activity in Rat Hippocampal Slices,” Brain Research, Vol. 998, No. 1, 2004, pp. 56-64. doi:10.1016/j.brainres.2003.11.010
L. Velísek, J. Velísková and P. K. Stanton, “Low-Frequency Stimulation of the Kindling Focus Delays Basolateralamygdala Kindling Inimmature Rats,” Neuroscience Letters, Vol. 326, No. 1, 2002, pp. 61-63. doi:10.1016/S0304-3940(02)00294-X
S. R. Weiss, A. Eidsath, X. L. Li, T. Heynen and R. M. Post, “Quenching Revisited: Low Level Direct Current Inhibits Amygdala-Kindled Seizures,” Experimental Neurology, Vol. 154, No. 1, 1998, pp. 185-192. doi:10.1006/exnr.1998.6932
M. Schubert, H. Siegmund, H. C. Pape and D. Albrecht, “Kindling-Induced Changes in Plasticity of the Rat Amygdala and Hippocampus,” Learning and Memory, Vol. 12, No. 5, 2005, pp. 520-526. doi:10.1101/lm.4205
T. V. Bliss and G. L. Collingridge, “A Synaptic Model of Memory: Long-Term Potentiation in the Hippocampus,” Nature, Vol. 361, No. 6407, 1993, pp. 31-39. doi:10.1038/361031a0
R. C. Malenka and R. A. Nicoll, “Long-Term Potentiation: A Decade of Progress?” Science, Vol. 285, No. 5435, 1999, pp. 1870-1874. doi:10.1126/science.285.5435.1870
C. J. Behrens, L. P. van den Boom, L. de Hoz, A. Friedman and U. Heinemann, “Induction of Sharp Wave-Ripple Complexes in Vitro and Reorganization of Hippocampal Networks,” Nature Neuroscience, Vol. 8, No. 11, 2005, pp. 1560-1567. doi:10.1038/nn1571