Local and Remote Chemogenetic Suppression of Hippocampal Seizures in Rats


Дәйексөз келтіру

Толық мәтін

Аннотация

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.

Авторлар туралы

Donghong Li

Department of Neurology, Third Affiliated Hospital, Sun Yat-sen University

Email: info@benthamscience.net

Xi Yan

Department of Neurology, Henan Provincial People’s Hospital, Zhengzhou University People’s Hospital, Henan University People’s Hospital

Email: info@benthamscience.net

Yue Xing

, Guangzhou Laboratory

Email: info@benthamscience.net

Jiaqing Yan

College of Electrical and Control Engineering, North China University of Technology

Email: info@benthamscience.net

Junling Wang

, Guangzhou Laboratory

Email: info@benthamscience.net

Herui Zhang

, Guangzhou Laboratory

Email: info@benthamscience.net

Jiaoyang Wang

, Guangzhou Laboratory

Email: info@benthamscience.net

Xiaonan Li

, Guangzhou Laboratory

Email: info@benthamscience.net

Zhumin Su

Department of Neurology, Third Affiliated Hospital,, Sun Yat-sen University

Email: info@benthamscience.net

Horace Loh

, Guangzhou Laboratory

Email: info@benthamscience.net

Xiaofeng Yang

, Guangzhou Laboratory

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Xiaohong Chen

Department of Neurology, Third Affiliated Hospital, Sun Yat-sen University

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Әдебиет тізімі

  1. Kwan, P.; Brodie, M.J. Early identification of refractory epilepsy. N. Engl. J. Med., 2000, 342(5), 314-319. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1073/pnas.0700293104 PMID: 17360345
  11. Roth, B.L. DREADDs for Neuroscientists. Neuron, 2016, 89(4), 683-694. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/S0140-6736(11)60890-8 PMID: 22000136
  46. Ryvlin, P. Beyond pharmacotherapy: Surgical management. Epilepsia, 2003, 44(Suppl. 5), 23-28. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.nbd.2022.105637 PMID: 35091040

Қосымша файлдар

Қосымша файлдар
Әрекет
1. JATS XML

© Bentham Science Publishers, 2024