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Current Neuropharmacology

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ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

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Research Article

Local and Remote Chemogenetic Suppression of Hippocampal Seizures in Rats

Author(s): Donghong Li, Xi Yan, Yue Xing, Jiaqing Yan, Junling Wang, Herui Zhang, Jiaoyang Wang, Xiaonan Li, Zhumin Su, Horace Hao Loh, Xiaofeng Yang* and Xiaohong Chen*

Volume 22, Issue 13, 2024

Published on: 07 February, 2024

Page: [2240 - 2255] Pages: 16

DOI: 10.2174/1570159X22999240131122455

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Innovative treatments of refractory epilepsy are widely desired, for which chemogenetic technology can provide region- and cell-type-specific modulation with relative noninvasiveness.

Objectives: We aimed to explore the specific applications of chemogenetics for locally and remotely networks controlling hippocampal seizures.

Methods: A virus coding for a modified human Gi-coupled M4 muscarinic receptor (hM4Di) on pyramidal cells was injected into either the right hippocampal CA3 or the bilateral anterior nucleus of the thalamus (ANT) in rats. After one month, seizures were induced by 4-aminopyridine (4-AP) injection into the right CA3. Simultaneously, clozapine-N-oxide (CNO) (2.5 mg/kg) or clozapine (0.1 mg/kg), the specific ligands acting on hM4Di, were injected intraperitoneally. We also set up hM4Di control and clozapine control groups to eliminate the influence of viral transfection and the ligand alone on the experimental results.

Results: For both local and remote controls, the mean seizure duration was significantly reduced upon ligand application in the experimental groups. Seizure frequency, on the other hand, only showed a significant decrease in local control, with a lower frequency in the clozapine group than in the CNO group. Both the effects of CNO and clozapine were time-dependent, and clozapine was faster than CNO in local seizure control.

Conclusion: This study shows the potency of chemogenetics to attenuate hippocampal seizures locally or remotely by activating the transfected hM4Di receptor with CNO or clozapine. ANT is suggested as a potentially safe chemogenetic application target in the epileptic network for focal hippocampal seizures.

Keywords: Chemogenetics, epileptic network, clozapine-N-oxide, clozapine, anterior nucleus, hippocampal seizures.

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[1]
Kwan, P.; Brodie, M.J. Early identification of refractory epilepsy. N. Engl. J. Med., 2000, 342(5), 314-319.
[http://dx.doi.org/10.1056/NEJM200002033420503] [PMID: 10660394]
[2]
Berg, A.T.; Berkovic, S.F.; Brodie, M.J.; Buchhalter, J.; Cross, J.H.; van Emde Boas, W.; Engel, J.; French, J.; Glauser, T.A.; Mathern, G.W.; Moshé, S.L.; Nordli, D.; Plouin, P.; Scheffer, I.E. Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia, 2010, 51(4), 676-685.
[http://dx.doi.org/10.1111/j.1528-1167.2010.02522.x] [PMID: 20196795]
[3]
Boon, P.; Vonck, K.; De Herdt, V.; Van Dycke, A.; Goethals, M.; Goossens, L.; Van Zandijcke, M.; De Smedt, T.; Dewaele, I.; Achten, R.; Wadman, W.; Dewaele, F.; Caemaert, J.; Van Roost, D. Deep brain stimulation in patients with refractory temporal lobe epilepsy. Epilepsia, 2007, 48(8), 1551-1560.
[http://dx.doi.org/10.1111/j.1528-1167.2007.01005.x] [PMID: 17726798]
[4]
Shiri, Z.; Manseau, F.; Lévesque, M.; Williams, S.; Avoli, M. Activation of specific neuronal networks leads to different seizure onset types. Ann. Neurol., 2016, 79(3), 354-365.
[http://dx.doi.org/10.1002/ana.24570] [PMID: 26605509]
[5]
Haberman, R.P.; Samulski, R.J.; McCown, T.J. Attenuation of seizures and neuronal death by adeno-associated virus vector galanin expression and secretion. Nat. Med., 2003, 9(8), 1076-1080.
[http://dx.doi.org/10.1038/nm901] [PMID: 12858168]
[6]
Noè, F.; Pool, A.H.; Nissinen, J.; Gobbi, M.; Bland, R.; Rizzi, M.; Balducci, C.; Ferraguti, F.; Sperk, G.; During, M.J.; Pitkänen, A.; Vezzani, A. Neuropeptide Y gene therapy decreases chronic spontaneous seizures in a rat model of temporal lobe epilepsy. Brain, 2008, 131(6), 1506-1515.
[http://dx.doi.org/10.1093/brain/awn079] [PMID: 18477594]
[7]
Keifer, O.; Kambara, K.; Lau, A.; Makinson, S.; Bertrand, D. Chemogenetics a robust approach to pharmacology and gene therapy. Biochem. Pharmacol., 2020, 175, 113889.
[http://dx.doi.org/10.1016/j.bcp.2020.113889] [PMID: 32119836]
[8]
Walker, M.C.; Kullmann, D.M. Optogenetic and chemogenetic therapies for epilepsy. Neuropharmacology, 2020, 168, 107751.
[http://dx.doi.org/10.1016/j.neuropharm.2019.107751] [PMID: 31494141]
[9]
Sternson, S.M.; Roth, B.L. Chemogenetic tools to interrogate brain functions. Annu. Rev. Neurosci., 2014, 37(1), 387-407.
[http://dx.doi.org/10.1146/annurev-neuro-071013-014048] [PMID: 25002280]
[10]
Armbruster, B.N.; Li, X.; Pausch, M.H.; Herlitze, S.; Roth, B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA, 2007, 104(12), 5163-5168.
[http://dx.doi.org/10.1073/pnas.0700293104] [PMID: 17360345]
[11]
Roth, B.L. DREADDs for Neuroscientists. Neuron, 2016, 89(4), 683-694.
[http://dx.doi.org/10.1016/j.neuron.2016.01.040] [PMID: 26889809]
[12]
Wiegert, J.S.; Mahn, M.; Prigge, M.; Printz, Y.; Yizhar, O. Silencing neurons: Tools, applications, and experimental constraints. Neuron, 2017, 95(3), 504-529.
[http://dx.doi.org/10.1016/j.neuron.2017.06.050] [PMID: 28772120]
[13]
Stachniak, T.J.; Ghosh, A.; Sternson, S.M. Chemogenetic synaptic silencing of neural circuits localizes a hypothalamus→midbrain pathway for feeding behavior. Neuron, 2014, 82(4), 797-808.
[http://dx.doi.org/10.1016/j.neuron.2014.04.008] [PMID: 24768300]
[14]
Kätzel, D.; Nicholson, E.; Schorge, S.; Walker, M.C.; Kullmann, D.M. Chemical–genetic attenuation of focal neocortical seizures. Nat. Commun., 2014, 5(1), 3847.
[http://dx.doi.org/10.1038/ncomms4847] [PMID: 24866701]
[15]
Wicker, E; Forcelli, PA Chemogenetic silencing of the midline and intralaminar thalamus blocks amygdala-kindled seizures. Exp. Neurol., 2016, 283(Pt A), 404-412.
[http://dx.doi.org/10.1016/j.expneurol.2016.07.003]
[16]
Wang, Y.; Xu, C.; Xu, Z.; Ji, C.; Liang, J.; Wang, Y.; Chen, B.; Wu, X.; Gao, F.; Wang, S.; Guo, Y.; Li, X.; Luo, J.; Duan, S.; Chen, Z. Depolarized GABAergic signaling in subicular microcircuits mediates generalized seizure in temporal lobe epilepsy. Neuron, 2017, 95(1), 92-105.e5.
[http://dx.doi.org/10.1016/j.neuron.2017.06.004] [PMID: 28648501]
[17]
Xu, C.; Wang, Y.; Zhang, S.; Nao, J.; Liu, Y.; Wang, Y.; Ding, F.; Zhong, K.; Chen, L.; Ying, X.; Wang, S.; Zhou, Y.; Duan, S.; Chen, Z. Subicular pyramidal neurons gate drug resistance in temporal lobe epilepsy. Ann. Neurol., 2019, 86(4), 626-640.
[http://dx.doi.org/10.1002/ana.25554] [PMID: 31340057]
[18]
Gomez, J.L.; Bonaventura, J.; Lesniak, W.; Mathews, W.B.; Sysa-Shah, P.; Rodriguez, L.A.; Ellis, R.J.; Richie, C.T.; Harvey, B.K.; Dannals, R.F.; Pomper, M.G.; Bonci, A.; Michaelides, M. Chemogenetics revealed: DREADD occupancy and activation via converted clozapine. Science, 2017, 357(6350), 503-507.
[http://dx.doi.org/10.1126/science.aan2475] [PMID: 28774929]
[19]
Manvich, D.F.; Webster, K.A.; Foster, S.L.; Farrell, M.S.; Ritchie, J.C.; Porter, J.H.; Weinshenker, D. The DREADD agonist clozapine N-oxide (CNO) is reverse-metabolized to clozapine and produces clozapine-like interoceptive stimulus effects in rats and mice. Sci. Rep., 2018, 8(1), 3840.
[http://dx.doi.org/10.1038/s41598-018-22116-z] [PMID: 29497149]
[20]
Oates, J.A.; Wood, A.J.J.; Baldessarini, R.J.; Frankenburg, F.R. Clozapine. N. Engl. J. Med., 1991, 324(11), 746-754.
[http://dx.doi.org/10.1056/NEJM199103143241107] [PMID: 1671793]
[21]
Desloovere, J.; Boon, P.; Larsen, L.E.; Merckx, C.; Goossens, M.G.; Van den Haute, C.; Baekelandt, V.; De Bundel, D.; Carrette, E.; Delbeke, J.; Meurs, A.; Vonck, K.; Wadman, W.; Raedt, R. Long‐term chemogenetic suppression of spontaneous seizures in a mouse model for temporal lobe epilepsy. Epilepsia, 2019, 60(11), 2314-2324.
[http://dx.doi.org/10.1111/epi.16368] [PMID: 31608439]
[22]
Avoli, M.; D’Antuono, M.; Louvel, J.; Köhling, R.; Biagini, G.; Pumain, R.; D’Arcangelo, G.; Tancredi, V. Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog. Neurobiol., 2002, 68(3), 167-207.
[http://dx.doi.org/10.1016/S0301-0082(02)00077-1] [PMID: 12450487]
[23]
Goldberg, E.M.; Coulter, D.A. Mechanisms of epileptogenesis: A convergence on neural circuit dysfunction. Nat. Rev. Neurosci., 2013, 14(5), 337-349.
[http://dx.doi.org/10.1038/nrn3482] [PMID: 23595016]
[24]
Khambhati, A.N.; Davis, K.A.; Oommen, B.S.; Chen, S.H.; Lucas, T.H.; Litt, B.; Bassett, D.S. Dynamic network drivers of seizure generation, propagation and termination in human neocortical epilepsy. PLOS Comput. Biol., 2015, 11(12), e1004608.
[http://dx.doi.org/10.1371/journal.pcbi.1004608] [PMID: 26680762]
[25]
Child, N.D.; Benarroch, E.E. Anterior nucleus of the thalamus: Functional organization and clinical implications. Neurology, 2013, 81(21), 1869-1876.
[http://dx.doi.org/10.1212/01.wnl.0000436078.95856.56] [PMID: 24142476]
[26]
Hamani, C.; Ewerton, F.I.S.; Bonilha, S.M.; Ballester, G.; Mello, L.E.A.M.; Lozano, A.M. Bilateral anterior thalamic nucleus lesions and high-frequency stimulation are protective against pilocarpine-induced seizures and status epilepticus. Neurosurgery, 2004, 54(1), 191-197.
[http://dx.doi.org/10.1227/01.NEU.0000097552.31763.AE] [PMID: 14683557]
[27]
Takebayashi, S.; Hashizume, K.; Tanaka, T.; Hodozuka, A. The effect of electrical stimulation and lesioning of the anterior thalamic nucleus on kainic acid-induced focal cortical seizure status in rats. Epilepsia, 2007, 48(2), 348-358.
[http://dx.doi.org/10.1111/j.1528-1167.2006.00948.x] [PMID: 17295630]
[28]
Oikawa, H.; Sasaki, M.; Tamakawa, Y.; Kamei, A. The circuit of Papez in mesial temporal sclerosis: MRI. Neuroradiology, 2001, 43(3), 205-210.
[http://dx.doi.org/10.1007/s002340000463] [PMID: 11305751]
[29]
Osorio, I.; Overman, J.; Giftakis, J.; Wilkinson, S.B. High frequency thalamic stimulation for inoperable mesial temporal epilepsy. Epilepsia, 2007, 48(8), 1561-1571.
[http://dx.doi.org/10.1111/j.1528-1167.2007.01044.x] [PMID: 17386053]
[30]
Zumsteg, D.; Lozano, A.M.; Wennberg, R.A. Mesial temporal inhibition in a patient with deep brain stimulation of the anterior thalamus for epilepsy. Epilepsia, 2006, 47(11), 1958-1962.
[http://dx.doi.org/10.1111/j.1528-1167.2006.00824.x] [PMID: 17116040]
[31]
Fisher, R.; Salanova, V.; Witt, T.; Worth, R.; Henry, T.; Gross, R.; Oommen, K.; Osorio, I.; Nazzaro, J.; Labar, D.; Kaplitt, M.; Sperling, M.; Sandok, E.; Neal, J.; Handforth, A.; Stern, J.; DeSalles, A.; Chung, S.; Shetter, A.; Bergen, D.; Bakay, R.; Henderson, J.; French, J.; Baltuch, G.; Rosenfeld, W.; Youkilis, A.; Marks, W.; Garcia, P.; Barbaro, N.; Fountain, N.; Bazil, C.; Goodman, R.; McKhann, G.; Babu Krishnamurthy, K.; Papavassiliou, S.; Epstein, C.; Pollard, J.; Tonder, L.; Grebin, J.; Coffey, R.; Graves, N. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia, 2010, 51(5), 899-908.
[http://dx.doi.org/10.1111/j.1528-1167.2010.02536.x] [PMID: 20331461]
[32]
Yu, T.; Wang, X.; Li, Y.; Zhang, G.; Worrell, G.; Chauvel, P.; Ni, D.; Qiao, L.; Liu, C.; Li, L.; Ren, L.; Wang, Y. High-frequency stimulation of anterior nucleus of thalamus desynchronizes epileptic network in humans. Brain, 2018, 141(9), 2631-2643.
[http://dx.doi.org/10.1093/brain/awy187] [PMID: 29985998]
[33]
Kerrigan, J.F.; Litt, B.; Fisher, R.S.; Cranstoun, S.; French, J.A.; Blum, D.E.; Dichter, M.; Shetter, A.; Baltuch, G.; Jaggi, J.; Krone, S.; Brodie, M.; Rise, M.; Graves, N. Electrical stimulation of the anterior nucleus of the thalamus for the treatment of intractable epilepsy. Epilepsia, 2004, 45(4), 346-354.
[http://dx.doi.org/10.1111/j.0013-9580.2004.01304.x] [PMID: 15030497]
[34]
Chen, N.; Yan, N.; Liu, C.; Ge, Y.; Zhang, J.G.; Meng, F.G. Neuroprotective effects of electrical stimulation of the anterior nucleus of the thalamus for hippocampus neurons in intractable epilepsy. Med. Hypotheses, 2013, 80(5), 517-519.
[http://dx.doi.org/10.1016/j.mehy.2013.02.002] [PMID: 23481284]
[35]
Paxinos, G.; Watson, C. The rat brain in stereotaxic coordinates, 6th ed; Academic Press/Elsevier: Amsterdam, Boston, 2007.
[36]
Vorhees, C.V.; Williams, M.T. Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat. Protoc., 2006, 1(2), 848-858.
[http://dx.doi.org/10.1038/nprot.2006.116] [PMID: 17406317]
[37]
Velascol, A.L.; Wilson, C.L.; Babb, T.L.; Engel, J., Jr Functional and anatomic correlates of two frequently observed temporal lobe seizure-onset patterns. Neural Plast., 2000, 7(1-2), 49-63.
[http://dx.doi.org/10.1155/NP.2000.49] [PMID: 10709214]
[38]
Perucca, P.; Dubeau, F.; Gotman, J. Intracranial electroencephalographic seizure-onset patterns: Effect of underlying pathology. Brain, 2014, 137(1), 183-196.
[http://dx.doi.org/10.1093/brain/awt299] [PMID: 24176980]
[39]
Epi, P.M.C. A roadmap for precision medicine in the epilepsies. Lancet Neurol., 2015, 14(12), 1219-1228.
[http://dx.doi.org/10.1016/S1474-4422(15)00199-4] [PMID: 26416172]
[40]
Téllez-Zenteno, J.F.; Dhar, R.; Wiebe, S. Long-term seizure outcomes following epilepsy surgery: A systematic review and meta-analysis. Brain, 2005, 128(5), 1188-1198.
[http://dx.doi.org/10.1093/brain/awh449] [PMID: 15758038]
[41]
Boyden, E.S.; Zhang, F.; Bamberg, E.; Nagel, G.; Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci., 2005, 8(9), 1263-1268.
[http://dx.doi.org/10.1038/nn1525] [PMID: 16116447]
[42]
Forcelli, P.A. Applications of optogenetic and chemogenetic methods to seizure circuits: Where to go next? J. Neurosci. Res., 2017, 95(12), 2345-2356.
[http://dx.doi.org/10.1002/jnr.24135] [PMID: 28791729]
[43]
Spencer, S.; Huh, L. Outcomes of epilepsy surgery in adults and children. Lancet Neurol., 2008, 7(6), 525-537.
[http://dx.doi.org/10.1016/S1474-4422(08)70109-1] [PMID: 18485316]
[44]
Sperling, M.R.; O’Connor, M.J.; Saykin, A.J.; Plummer, C. Temporal lobectomy for refractory epilepsy. JAMA, 1996, 276(6), 470-475.
[http://dx.doi.org/10.1001/jama.1996.03540060046034] [PMID: 8691555]
[45]
de Tisi, J.; Bell, G.S.; Peacock, J.L.; McEvoy, A.W.; Harkness, W.F.J.; Sander, J.W.; Duncan, J.S. The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: A cohort study. Lancet, 2011, 378(9800), 1388-1395.
[http://dx.doi.org/10.1016/S0140-6736(11)60890-8] [PMID: 22000136]
[46]
Ryvlin, P. Beyond pharmacotherapy: Surgical management. Epilepsia, 2003, 44(Suppl. 5), 23-28.
[http://dx.doi.org/10.1046/j.1528-1157.44.s.5.4.x] [PMID: 12859359]
[47]
Guye, M.; Régis, J.; Tamura, M.; Wendling, F.; McGonigal, A.; Chauvel, P.; Bartolomei, F. The role of corticothalamic coupling in human temporal lobe epilepsy. Brain, 2006, 129(7), 1917-1928.
[http://dx.doi.org/10.1093/brain/awl151] [PMID: 16760199]
[48]
Ferreira, E.S.; Vieira, L.G.; Moraes, D.M.; Amorim, B.O.; Malheiros, J.M.; Hamani, C.; Covolan, L. Long-term effects of anterior thalamic nucleus deep brain stimulation on spatial learning in the pilocarpine model of temporal lobe epilepsy. Neuromodulation, 2018, 21(2), 160-167.
[http://dx.doi.org/10.1111/ner.12688] [PMID: 28960670]
[49]
Covolan, L.; de Almeida, A.C.G.; Amorim, B.; Cavarsan, C.; Miranda, M.F.; Aarão, M.C.; Madureira, A.P.; Rodrigues, A.M.; Nobrega, J.N.; Mello, L.E.; Hamani, C. Effects of anterior thalamic nucleus deep brain stimulation in chronic epileptic rats. PLoS One, 2014, 9(6), e97618.
[http://dx.doi.org/10.1371/journal.pone.0097618] [PMID: 24892420]
[50]
Williamson, A.; Patrylo, P.R.; Pan, J.; Spencer, D.D.; Hetherington, H. Correlations between granule cell physiology and bioenergetics in human temporal lobe epilepsy. Brain, 2005, 128(5), 1199-1208.
[http://dx.doi.org/10.1093/brain/awh444] [PMID: 15728655]
[51]
Wang, Y.; Liang, J.; Chen, L.; Shen, Y.; Zhao, J.; Xu, C.; Wu, X.; Cheng, H.; Ying, X.; Guo, Y.; Wang, S.; Zhou, Y.; Wang, Y.; Chen, Z. Pharmaco-genetic therapeutics targeting parvalbumin neurons attenuate temporal lobe epilepsy. Neurobiol. Dis., 2018, 117, 149-160.
[http://dx.doi.org/10.1016/j.nbd.2018.06.006] [PMID: 29894753]
[52]
Liu, J.; Yu, T.; Wu, J.; Pan, Y.; Tan, Z.; Liu, R.; Wang, X.; Ren, L.; Wang, L. Anterior thalamic stimulation improves working memory precision judgments. Brain Stimul., 2021, 14(5), 1073-1080.
[http://dx.doi.org/10.1016/j.brs.2021.07.006] [PMID: 34284167]
[53]
Wolff, M.; Gibb, S.J.; Dalrymple-Alford, J.C. Beyond spatial memory: The anterior thalamus and memory for the temporal order of a sequence of odor cues. J. Neurosci., 2006, 26(11), 2907-2913.
[http://dx.doi.org/10.1523/JNEUROSCI.5481-05.2006] [PMID: 16540567]
[54]
Salanova, V.; Witt, T.; Worth, R.; Henry, T.R.; Gross, R.E.; Nazzaro, J.M.; Labar, D.; Sperling, M.R.; Sharan, A.; Sandok, E.; Handforth, A.; Stern, J.M.; Chung, S.; Henderson, J.M.; French, J.; Baltuch, G.; Rosenfeld, W.E.; Garcia, P.; Barbaro, N.M.; Fountain, N.B.; Elias, W.J.; Goodman, R.R.; Pollard, J.R.; Tröster, A.I.; Irwin, C.P.; Lambrecht, K.; Graves, N.; Fisher, R. Long-term efficacy and safety of thalamic stimulation for drug-resistant partial epilepsy. Neurology, 2015, 84(10), 1017-1025.
[http://dx.doi.org/10.1212/WNL.0000000000001334] [PMID: 25663221]
[55]
Shi, L.; Yang, A.C.; Li, J.J.; Meng, D.W.; Jiang, B.; Zhang, J.G. Favorable modulation in neurotransmitters: Effects of chronic anterior thalamic nuclei stimulation observed in epileptic monkeys. Exp. Neurol., 2015, 265, 94-101.
[http://dx.doi.org/10.1016/j.expneurol.2015.01.003] [PMID: 25596526]
[56]
Hartikainen, K.M.; Sun, L.; Polvivaara, M.; Brause, M.; Lehtimäki, K.; Haapasalo, J.; Möttönen, T.; Väyrynen, K.; Ogawa, K.H.; Öhman, J.; Peltola, J. Immediate effects of deep brain stimulation of anterior thalamic nuclei on executive functions and emotion–attention interaction in humans. J. Clin. Exp. Neuropsychol., 2014, 36(5), 540-550.
[http://dx.doi.org/10.1080/13803395.2014.913554] [PMID: 24839985]
[57]
Zhang, S.; Gumpper, R.H.; Huang, X.P.; Liu, Y.; Krumm, B.E.; Cao, C.; Fay, J.F.; Roth, B.L. Molecular basis for selective activation of DREADD-based chemogenetics. Nature, 2022, 612(7939), 354-362.
[http://dx.doi.org/10.1038/s41586-022-05489-0] [PMID: 36450989]
[58]
Weston, M; Kaserer, T; Wu, A; Mouravlev, A; Carpenter, JC Snowball, A Olanzapine: A potent agonist at the hM4D(Gi) DREADD amenable to clinical translation of chemogenetics. Sci Adv, 2019, 5(4), eaaw1567.
[59]
Bender, D.; Holschbach, M.; Stöcklin, G. Synthesis of n.c.a. carbon-11 labelled clozapine and its major metabolite clozapine-N-oxide and comparison of their biodistribution in mice. Nucl. Med. Biol., 1994, 21(7), 921-925.
[http://dx.doi.org/10.1016/0969-8051(94)90080-9] [PMID: 9234345]
[60]
Jann, M.W.; Lam, Y.W.; Chang, W.H. Rapid formation of clozapine in guinea-pigs and man following clozapine-N-oxide administration. Arch. Int. Pharmacodyn. Ther., 1994, 328(2), 243-250.
[PMID: 7710309]
[61]
Sajatovic, M.; Meltzer, H.Y. Clozapine-induced myoclonus and generalized seizures. Biol. Psychiatry, 1996, 39(5), 367-370.
[http://dx.doi.org/10.1016/0006-3223(95)00499-8] [PMID: 8704069]
[62]
Koch-Stoecker, S. Antipsychotic drugs and epilepsy: Indications and treatment guidelines. Epilepsia, 2002, 43(s2), 19-24.
[http://dx.doi.org/10.1046/j.1528-1157.2002.043s2019.x] [PMID: 11903478]
[63]
Wenthur, C.J.; Lindsley, C.W. Classics in chemical neuroscience. Clozapine. ACS Chem. Neurosci., 2013, 4(7), 1018-1025.
[http://dx.doi.org/10.1021/cn400121z] [PMID: 24047509]
[64]
Vardy, E.; Robinson, J.E.; Li, C.; Olsen, R.H.J.; DiBerto, J.F.; Giguere, P.M.; Sassano, F.M.; Huang, X.P.; Zhu, H.; Urban, D.J.; White, K.L.; Rittiner, J.E.; Crowley, N.A.; Pleil, K.E.; Mazzone, C.M.; Mosier, P.D.; Song, J.; Kash, T.L.; Malanga, C.J.; Krashes, M.J.; Roth, B.L. A new DREADD facilitates the multiplexed chemogenetic interrogation of behavior. Neuron, 2015, 86(4), 936-946.
[http://dx.doi.org/10.1016/j.neuron.2015.03.065] [PMID: 25937170]
[65]
Stypulkowski, P.H.; Stanslaski, S.R.; Jensen, R.M.; Denison, T.J.; Giftakis, J.E. Brain stimulation for epilepsy--local and remote modulation of network excitability. Brain Stimul., 2014, 7(3), 350-358.
[http://dx.doi.org/10.1016/j.brs.2014.02.002] [PMID: 24613614]
[66]
Fujita, S.; Toyoda, I.; Thamattoor, A.K.; Buckmaster, P.S. Preictal activity of subicular, CA1, and dentate gyrus principal neurons in the dorsal hippocampus before spontaneous seizures in a rat model of temporal lobe epilepsy. J. Neurosci., 2014, 34(50), 16671-16687.
[http://dx.doi.org/10.1523/JNEUROSCI.0584-14.2014] [PMID: 25505320]
[67]
Park, S.C.; Lee, S.K.; Chung, C.K. Quantitative peri-ictal electrocorticography and long-term seizure outcomes in temporal lobe epilepsy. Epilepsy Res., 2015, 109, 169-182.
[http://dx.doi.org/10.1016/j.eplepsyres.2014.10.005] [PMID: 25524857]
[68]
Ren, G.; Yan, J.; Tao, G.; Gan, Y.; Li, D.; Yan, X.; Fu, Y.; Wang, L.; Wang, W.; Zhang, Z.; Yue, F.; Yang, X. Rapid focal cooling attenuates cortical seizures in a primate epilepsy model. Exp. Neurol., 2017, 295, 202-210.
[http://dx.doi.org/10.1016/j.expneurol.2017.06.008] [PMID: 28601605]
[69]
Wang, Y.; Liang, J.; Xu, C.; Wang, Y.; Kuang, Y.; Xu, Z.; Guo, Y.; Wang, S.; Gao, F.; Chen, Z. Low-frequency stimulation in anterior nucleus of thalamus alleviates kainate-induced chronic epilepsy and modulates the hippocampal EEG rhythm. Exp. Neurol., 2016, 276, 22-30.
[http://dx.doi.org/10.1016/j.expneurol.2015.11.014] [PMID: 26621617]
[70]
Jutras, M.J.; Fries, P.; Buffalo, E.A. Gamma-band synchronization in the macaque hippocampus and memory formation. J. Neurosci., 2009, 29(40), 12521-12531.
[http://dx.doi.org/10.1523/JNEUROSCI.0640-09.2009] [PMID: 19812327]
[71]
Montgomery, S.M.; Buzsáki, G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc. Natl. Acad. Sci. USA, 2007, 104(36), 14495-14500.
[http://dx.doi.org/10.1073/pnas.0701826104] [PMID: 17726109]
[72]
Isomura, Y.; Sirota, A.; Özen, S.; Montgomery, S.; Mizuseki, K.; Henze, D.A.; Buzsáki, G. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron, 2006, 52(5), 871-882.
[http://dx.doi.org/10.1016/j.neuron.2006.10.023] [PMID: 17145507]
[73]
Csicsvari, J.; Jamieson, B.; Wise, K.D.; Buzsáki, G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron, 2003, 37(2), 311-322.
[http://dx.doi.org/10.1016/S0896-6273(02)01169-8] [PMID: 12546825]
[74]
Parra, J.; Kalitzin, S.N.; Iriarte, J.; Blanes, W.; Velis, D.N.; Lopes da Silva, F.H. Gamma-band phase clustering and photosensitivity: Is there an underlying mechanism common to photosensitive epilepsy and visual perception? Brain, 2003, 126(5), 1164-1172.
[http://dx.doi.org/10.1093/brain/awg109] [PMID: 12690055]
[75]
Avoli, M.; de Curtis, M.; Gnatkovsky, V.; Gotman, J.; Köhling, R.; Lévesque, M.; Manseau, F.; Shiri, Z.; Williams, S. Specific imbalance of excitatory/inhibitory signaling establishes seizure onset pattern in temporal lobe epilepsy. J. Neurophysiol., 2016, 115(6), 3229-3237.
[http://dx.doi.org/10.1152/jn.01128.2015] [PMID: 27075542]
[76]
Bragin, A.; Azizyan, A.; Almajano, J.; Engel, J., Jr The cause of the imbalance in the neuronal network leading to seizure activity can be predicted by the electrographic pattern of the seizure onset. J. Neurosci., 2009, 29(11), 3660-3671.
[http://dx.doi.org/10.1523/JNEUROSCI.5309-08.2009] [PMID: 19295168]
[77]
Bragin, A.; Engel, J., Jr; Wilson, C.L.; Vizentin, E.; Mathern, G.W. Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia, 1999, 40(9), 1210-1221.
[http://dx.doi.org/10.1111/j.1528-1157.1999.tb00849.x] [PMID: 10487183]
[78]
Lisgaras, C.P.; Scharfman, H.E. Robust chronic convulsive seizures, high frequency oscillations, and human seizure onset patterns in an intrahippocampal kainic acid model in mice. Neurobiol. Dis., 2022, 166, 105637.
[http://dx.doi.org/10.1016/j.nbd.2022.105637] [PMID: 35091040]

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