Low frequency stimulation of ventral hippocampal commissures reduces seizures in a rat model of chronic temporal lobe epilepsy

Epilepsia

Volumn 53, Issue 1, 2012, Pages 147-156

  Rashid, Saifur ^a,c   Pho, Gerald ^a   Czigler, Michael ^a   Werz, Mary A ^b,d   Durand, Dominique M ^a  

^a Case Western Reserve University   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

Amygdala; Brain stimulation; Deep brain stimulation; Low frequency stimulation; Temporal lobe epilepsy; Ventral hippocampal commissure

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; BRAIN DEPTH STIMULATION; BRAIN HEMORRHAGE; BRAIN INFECTION; CONTROLLED STUDY; DENTATE GYRUS; ELECTRODE; EPILEPTIC STATE; EXCITABILITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HISTOPATHOLOGY; LOW FREQUENCY STIMULATION; MALE; NERVE CELL LESION; NERVOUS TISSUE; NEUROLOGICAL COMPLICATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPIKE; TEMPORAL LOBE EPILEPSY; THERAPY EFFECT; TREATMENT DURATION; VENTRAL HIPPOCAMPAL COMMISSURE;

ANIMALS; CA3 REGION, HIPPOCAMPAL; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ELECTRIC STIMULATION THERAPY; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; TREATMENT OUTCOME;

EID: 84855419634     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2011.03348.x     Document Type: Article

References (69)

1. Adjouadi MD, Sanchez M, Cabrerizo M, Ayala P, Jayakar I, Yaylali A, Barreto A,. (2004) Interictal spike detection using the Walsh transform. IEEE Trans Biomed Eng 51: 868-872. (Pubitemid 38525723)
2. Albensi BC, Ata G, Schmidt E, Waterman JD, Janigro D,. (2004) Activation of long-term synaptic plasticity causes suppression of epileptiform activity in rat hippocampal slices. Brain Res 998: 56-64. (Pubitemid 38077126)
3. Avoli M, D'Antuono M, Louvel J, Kohling R, Biagini G, Pumain R, D'Arcangelo G, Tancredi V,. (2002) Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog Neurobiol 68: 167-207.
4. Benabid AL, Pollak P, Gao D, Hoffmann D, Limousin P, Gay E, Payen I, Benazzouz A,. (1996) Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg 84: 203-214. (Pubitemid 26039470)
5. Blackstad TW,. (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105: 417-537.
6. Cavalheiro EA, Leite JP, Bortolotto ZA, Turski WA, Ikonomidou C, Turski L,. (1991) Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 32: 778-782.
7. Chkhenkeli SA, Sramka M, Lortkipanidze GS, Rakviashvili TN, Bregvadze ESh, Magalashvili GE, Gagoshidze TSh, Chkhenkeli IS,. (2004) Electrophysiological effects and clinical results of direct brain stimulation for intractable epilepsy. Clin Neurol Neurosurg 106: 318-329. (Pubitemid 39024633)
8. Colnat-Coulbois S, Mok K, Klein D, Pénicaud S, Tanriverdi T, Olivier A,. (2010) Tractography of the amygdala and hippocampus: anatomical study and application to selective amygdalohippocampectomy. J Neurosurg 113: 1135-1143.
9. Concha L, Gross DW, Wheatley BM, Beaulieu C,. (2006) Diffusion tensor imaging of time-dependent axonal and myelin degradation after corpus callosotomy in epilepsy patients. Neuroimage 32: 1090-1099. (Pubitemid 44278665)
10. de Curtis M, Avanzini G,. (2001) Interictal spikes in focal epileptogenesis. Prog Neurobiol 63: 541-567. (Pubitemid 32115432)
11. Deep Brain Stimulation for Parkinson's Disease Study Group. (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med 345: 956-963.
12. Dichter MA, Ayala GF,. (1987) Cellular mechanisms of epilepsy: a status report. Science 237: 157-164. (Pubitemid 17095917)
13. Dostrovsky JO, Lozano AM,. (2002) Mechanisms of deep brain stimulation. Mov Disord 17 (Suppl. 3): S63-S68. (Pubitemid 36040906)
14. Durand DM, Bikson M,. (2001) Suppression and control of epileptiform activity by electrical stimulation: a review. Proc IEEE 89: 1065-1082.
15. 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, SANTE Study Group. (2010) Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia 51: 899-908.
16. Gabriëls L, Cosyns P, Nuttin B, Demeulemeester H, Gybels J,. (2003) Deep brain stimulation for treatment-refractory obsessive-compulsive disorder: psychopathological and neuropsychological outcome in three cases. Acta Psychiatr Scand 107: 275-282. (Pubitemid 36458211)
17. Gloor P, Salanova V, Olivier A, Quesney LF,. (1993) The human dorsal hippocampal commissure. An anatomically identifiable and functional pathway. Brain 116: 1249-1273. (Pubitemid 23329892)
18. Goddard GV, McIntyre DC, Leech CK,. (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25: 295-330.
19. Goodman JH, Berger RE, Tcheng TK,. (2005) Preemptive low-frequency stimulation decreases the incidence of amygdala-kindled seizures. Epilepsia 46: 1-7. (Pubitemid 40179926)
20. Gotman J,. (1987) Interhemispheric interactions in seizures of focal onset: data from human intracranial recordings. Electroencephalogr Clin Neurophysiol 67: 120-133. (Pubitemid 17096044)
21. Gottlieb DI, Cowan WM,. (1973) Autoradiographic studies of the commissural and ipsilateral association connection of the hippocampus and detentate gyrus of the rat. I. The commissural connections. J Comp Neurol 149: 393-422.
22. Heck C,. (2010) Long term follow-up of the RNS(TM) system in adults with medically intractable partial onset seizures. AES, San Antonio, Texas.
23. Hodaie M, Wennberg RA, Dostrovsky JO, Lozano AM,. (2002) Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia 43: 603-608. (Pubitemid 34627719)
24. Holtzheimer PE, Mayberg HS,. (2010) Deep brain stimulation for treatment-resistant depression. Am J Psychiatry 167: 1437-1444.
25. Hufnagel A, Dümpelmann M, Zentner J, Schijns O, Elger CE,. (2000) Clinical relevance of quantified intracranial interictal spike activity in presurgical evaluation of epilepsy. Epilepsia 41: 467-478. (Pubitemid 30196615)
26. Jefferys JG,. (1990) Basic mechanisms of focal epilepsies. Exp Physiol 75: 127-162.
27. Jerger K, Schiff SJ,. (1995) Periodic pacing an in vitro epileptic focus. J Neurophysiol 73: 876-879.
28. Jobst BC, Darcey TM, Thadani VM, Roberts DW,. (2010) Brain stimulation for the treatment of epilepsy. Epilepsia 51 (Suppl. 3): 88-92.
29. Kile KB, Tian N, Durand DM,. (2008) Scn2a sodium channel mutation results in hyperexcitability in the hippocampus in vitro. Epilepsia 49: 488-499. (Pubitemid 351294533)
30. Kile KB, Tian N, Durand DM,. (2010) Low frequency stimulation decreases seizure activity in a mutation model of epilepsy. Epilepsia 51: 1745-1753.
31. Kinoshita M, Ikeda A, Matsuhashi M, Matsumoto R, Hitomi T, Begum T, Usui K, Takayama M, Mikuni N, Miyamoto S, Hashimoto N, Shibasaki H,. (2005) Electric cortical stimulation suppresses epileptic and background activities in neocortical epilepsy and mesial temporal lobe epilepsy. Clin Neurophysiol 116: 1291-1299. (Pubitemid 40839338)
32. Koubeissi MZ, Durand D, Rashid S, Syed T, Maciunas R, Luders H,. (2009) In vivo demonstration of connectivity between dorsal hippocampal commissure and bilateral mesial temporal structures. 63rd Annual Meeting of the American Epilepsy Society, Boston.
33. Laurberg S,. (1979) Commissural and intrinsic connections of the rat hippocampus. J Comp Neurol 184: 685-708. (Pubitemid 9149944)
34. Leite JP, Bortolotto ZA, Cavalheiro EA,. (1990) Spontaneous recurrent seizures in rats: an experimental model of partial epilepsy. Neurosci Biobehav Rev 14: 511-517.
35. Lieb JP, Hoque K, Skomer CE, Song XW,. (1987) Inter-hemispheric propagation of human mesial temporal lobe seizures: a coherence/phase analysis. Electroencephalogr Clin Neurophysiol 67: 101-119. (Pubitemid 17096043)
36. Lõpez-Meraz ML, Neri-Bazán L, Rocha L,. (2004) Low frequency stimulation modifies receptor binding in rat brain. Epilepsy Res 59: 95-105. (Pubitemid 38898669)
37. Lothman EW, Bertram EH, Bekenstein JW, Perlin JB,. (1989) Self-sustaining limbic status epilepticus induced by "continuous" hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res 3: 107-119. (Pubitemid 19071179)
38. Lothman EW, Bertram EH, Kapur J, Stringer JL,. (1990) Recurrent spontaneous hippocampal seizures in the rat as a chronic sequela to limbic status epilepticus. Epilepsy Res 6: 110-118. (Pubitemid 20184977)
39. Luders H,. (2004) Brain stimulation and epilepsy: novel approaches for seizure control. Suppl Clin Neurophysiol 57: 379-382.
40. McIntyre CC, Savasta M, Kerkerian-Le Goff L, Vitek JL,. (2004) Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol 115: 1239-1248. (Pubitemid 38596707)
41. Mogilner AY, Rezai AR,. (2003) Brain stimulation: history, current clinical application, and future prospects. Acta Neurochir Suppl 87: 115-120.
42. Mohammad-Zadeh M, Mirnajafi-Zadeh J, Fathollahi Y, Javan M, Jahanshahi A, Noorbakhsh SM, Motamedi F,. (2009) The role of adenosine A(1) receptors in mediating the inhibitory effects of low frequency stimulation of perforant path on kindling acquisition in rats. Neuroscience 158: 1632-1643.
43. Morrell M,. (2006) Brain stimulation for epilepsy: can scheduled or responsive neurostimulation stop seizures? Curr Opin Neurol 19: 164-168.
44. Morrell MJ,; RNS System in Epilepsy Study Group. (2011) Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology 77: 1295-1304.
45. Nail-Boucherie K, Lê-Pham BT, Marescaux C, Depaulis A,. (2002) Suppression of absence seizures by electrical and pharmacological activation of the caudal superior colliculus in a genetic model of absence epilepsy in the rat. Exp Neurol 177: 503-514. (Pubitemid 35366138)
46. Nissinen J, Pitkanen A,. (2007) Effect of antiepileptic drugs on spontaneous seizures in epileptic rats. Epilepsy Res 73: 181-191. (Pubitemid 46329332)
47. Nissinen J, Halonen T, Koivisto E, Pitkänen A,. (2000) A new model of chronic temporal lobe epilepsy induced by electrical stimulation of the amygdala in rat. Epilepsy Res 38: 177-205.
48. Ozen LJ, Young NA, Koshimori Y, Teskey GC,. (2008) Low-frequency stimulation reverses kindling-induced neocortical motor map expansion. Neuroscience 153: 300-307.
49. Parrent A, Almeida CS,. (2006) Deep brain stimulation and cortical stimulation in the treatment of epilepsy. Adv Neurol 97: 563-572.
50. Paxinos G, Watson C,. (2007) The rat brain stereotaxic coordinates. Academic Press, London.
51. Pitkänen A, Savander V, LeDoux JE,. (1997) Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 20: 517-523. (Pubitemid 27459657)
52. Racine RJ,. (1972) Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294.
53. Schiller Y, Bankirer Y,. (2007) Cellular mechanisms underlying antiepileptic effects of low- and high-frequency electrical stimulation in acute epilepsy in neocortical brain slices in vitro. J Neurophysiol 97: 1887-1902. (Pubitemid 46411179)
54. Schrader LM, Stern JM, Wilson CL, Fields TA, Salamon N, Nuwer MR, Vespa PM, Fried I,. (2006) Low frequency electrical stimulation through subdural electrodes in a case of refractory status epilepticus. Clin Neurophysiol 117: 781-788.
55. Spencer SS, Williamson PD, Spencer DD, Mattson RH,. (1987) Human hippocampal seizure spread studied by depth and subdural recording: the hippocampal commissure. Epilepsia 28: 479-489. (Pubitemid 17146595)
56. Spuck S, Tronnier V, Orosz I, Schönweiler R, Sepehrnia A, Nowak G, Sperner J,. (2010) Operative and technical complications of vagus nerve stimulator implantation. Neurosurgery 67: 489-494.
57. Stafstrom CE, Thompson JL, Holmes GL,. (1992) Kainic acid seizures in the developing brain: status epilepticus and spontaneous recurrent seizures. Brain Res Dev Brain Res 65: 227-236.
58. Swanson LW, Wyss JM, Cowan WM,. (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181: 681-715. (Pubitemid 9009540)
59. Theodore WH, Fisher RS,. (2004) Brain stimulation for epilepsy. Lancet Neurol 3: 111-118. (Pubitemid 38121314)
60. Velasco F, Velasco M, Velasco AL, Jimenez F, Marquez I, Rise M,. (1995) Electrical stimulation of the centromedian thalamic nucleus in control of seizures: long-term studies. Epilepsia 36: 63-71.
61. Velasco F, Velasco M, Velasco AL, Menez D, Rocha L,. (2001a) Electrical stimulation for epilepsy: stimulation of hippocampal foci. Stereotact Funct Neurosurg 77: 223-227.
62. Velasco M, Velasco F, Velasco AL,. (2001b) Centromedian-thalamic and hippocampal electrical stimulation for the control of intractable epileptic seizures. J Clin Neurophysiol 18: 495-513. (Pubitemid 34027846)
63. Velísek L, Velísková J, Stanton PK,. (2002) Low-frequency stimulation of the kindling focus delays basolateral amygdala kindling in immature rats. Neurosci Lett 326: 61-63. (Pubitemid 34607594)
64. Vidailhet M, Vercueil L, Houeto JL, Krystkowiak P, Benabid AL, Cornu P, Lagrange C, Tézenas du Montcel S, Dormont D, Grand S, Blond S, Detante O, Pillon B, Ardouin C, Agid Y, Destée A, Pollak P, French Stimulation du Pallidum Interne dans la Dystonie (SPIDY) Study Group. (2005) Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. N Engl J Med 352: 459-467. (Pubitemid 40175972)
65. Vitek JL,. (2002) Mechanisms of deep brain stimulation: excitation or inhibition. Mov Disord 17 (Suppl. 3): S69-S72. (Pubitemid 36040907)
66. Xu ZH, Wu DC, Fang Q, Zhong K, Wang S, Sun HL, Zhang SH, Chen Z,. (2010) Therapeutic time window of low-frequency stimulation at entorhinal cortex for amygdaloid-kindling seizures in rats. Epilepsia 51: 1861-1864.
67. Yang LX, Jin CL, Zhu-Ge ZB, Wang S, Wei EQ, Bruce IC, Chen Z,. (2006) Unilateral low-frequency stimulation of central piriform cortex delays seizure development induced by amygdaloid kindling in rats. Neuroscience 138: 1089-1096. (Pubitemid 43363527)
68. Zhang SH, Sun HL, Fang Q, Zhong K, Wu DC, Wang S, Chen Z,. (2009) Low-frequency stimulation of the hippocampal CA3 subfield is anti-epileptogenic and anti-ictogenic in rat amygdaloid kindling model of epilepsy. Neurosci Lett 455: 51-55.
69. Zumsteg D, Andrade DM, Wennberg RA,. (2006) Clinical electrophysiology factors indicative of intractability in patients with temporal lobe epilepsy. Adv Neurol 97: 45-62.