Effective inhibition of substantia nigra by deep brain stimulation fails to suppress tonic epileptic seizures

Neurobiology of Disease

Volumn 43, Issue 3, 2011, Pages 725-735

  Shehab, Safa ^a   Al Nahdi, Arwa ^a   Al Zaabi, Fatema ^a   Al Mugaddam, Fadwa ^a   Al Sultan, Mahmood ^a   Ljubisavljevic, Milos ^a  

^a UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

Author keywords

C fos; Deep brain stimulation; MES; Rat; Substantia nigra; Tonic seizures

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; MOLECULAR MARKER; NEURON SPECIFIC NUCLEAR PROTEIN; PARVALBUMIN; PROTEIN C FOS; PROTEIN IBA1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ATONIC SEIZURE; BRAIN DEPTH STIMULATION; CELL NUCLEUS; CONTROLLED STUDY; ELECTROSTIMULATION; HIGH FREQUENCY ELECTRICAL STIMULATION; IMMUNOCYTOCHEMISTRY; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RHOMBENCEPHALON; SUBSTANTIA NIGRA; TREATMENT FAILURE;

ANESTHESIA; ANESTHETICS, INHALATION; ANIMALS; DEEP BRAIN STIMULATION; EPILEPSY, TONIC-CLONIC; ETHER, ETHYL; MALE; NEURAL INHIBITION; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; TREATMENT FAILURE;

EID: 79960244817     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.06.002     Document Type: Article

References (69)

1. Applegate C.D., Pretel S., Piekut D.T. The substantia nigra pars reticulata, seizures and Fos expression. Epilepsy Res. 1995, 20:31-39.
2. Benabid A.L., Wallace B., Mitrofanis J., Xia R., Piallat B., Chabardes S., Berger F. A putative generalized model of the effects and mechanism of action of high frequency electrical stimulation of the central nervous system. Acta Neurol. Belg. 2005, 105:149-157.
3. Benazzouz A., Piallat B., Pollak P., Benabid A.L. Responses of substantia nigra pars reticulata and globus pallidus complex to high frequency stimulation of the subthalamic nucleus in rats: electrophysiological data. Neurosci. Lett. 1995, 189:77-80.
4. Benazzouz A., Gao D.M., Ni Z.G., Piallat B., Bouali-Benazzouz R., Benabid A.L. Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neuroscience 2000, 99:289-295.
5. Boex C., Vulliemoz S., Spinelli L., Pollo C., Seeck M. High and low frequency electrical stimulation in non-lesional temporal lobe epilepsy. Seizure 2007, 16:664-669.
6. Browning R.A., Nelson D.K. Modification of electroshock and pentylenetetrazol seizure patterns in rats after precollicular transections. Exp. Neurol. 1986, 93:546-556.
7. Bullitt E. Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J. Comp. Neurol. 1990, 296:517-530.
8. Chabardes S., Kahane P., Minotti L., Koudsie A., Hirsch E., Benabid A.L. Deep brain stimulation in epilepsy with particular reference to the subthalamic nucleus. Epileptic Disord. 2002, 4(Suppl. 3):S83-S93.
9. Cooper I.S., Amin I., Riklan M., Waltz J.M., Poon T.P. Chronic cerebellar stimulation in epilepsy. Clinical and anatomical studies. Arch. Neurol. 1976, 33:559-570.
10. Deniau J.M., Degos B., Bosch C., Maurice N. Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. Eur. J. Neurosci. 2010, 32:1080-1091.
11. Depaulis A., Vergnes M., Marescaux C. Endogenous control of epilepsy: the nigral inhibitory system. Prog. Neurobiol. 1994, 42:33-52.
12. Deransart C., Marescaux C., Depaulis A. Involvement of nigral glutamatergic inputs in the control of seizures in a genetic model of absence epilepsy in the rat. Neuroscience 1996, 71:721-728.
13. Deransart C., Le B.T., Marescaux C., Depaulis A. Role of the subthalamo-nigral input in the control of amygdala-kindled seizures in the rat. Brain Res. 1998, 807:78-83.
14. Deransart C., Le Pham B.T., Hirsch E., Marescaux C., Depaulis A. Inhibition of the substantia nigra suppresses absences and clonic seizures in audiogenic rats, but not tonic seizures: evidence for seizure specificity of the nigral control. Neuroscience 2001, 105:203-211.
15. Dragunow M., Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 1989, 29:261-265.
16. Dybdal D., Gale K. Postural and anticonvulsant effects of inhibition of the rat subthalamic nucleus. J. Neurosci. 2000, 20:6728-6733.
17. Feddersen B., Vercueil L., Noachtar S., David O., Depaulis A., Deransart C. Controlling seizures is not controlling epilepsy: a parametric study of deep brain stimulation for epilepsy. Neurobiol. Dis. 2007, 27:292-300.
18. Fisher R.S. Animal models of the epilepsies. Brain Res. Brain Res. Rev. 1989, 14:245-278.
19. Gale K. Progression and generalization of seizure discharge: anatomical and neurochemical substrates. Epilepsia 1988, 29(Suppl. 2):S15-S34.
20. Gale K., Browning R.A. Anatomical and neurochemical substrates of clonic and tonic seizures. Mechanisms of Epileptogenesis: The Transition to Seizure 1988, 111-152. Plenum Press, New York and London. M.A. Dichter (Ed.).
21. Garant D.S., Gale K. Substantia nigra-mediated anticonvulsant actions: role of nigral output pathways. Exp. Neurol. 1987, 97:143-159.
22. Gerfen C.R., Wilson C.J. The basal ganglia. Integrated systems of the CNS, Part III 1996, 371-468. Elsevier, Amsterdam. L.W. Swanson, A. Bjorklund, T. Hokfelt (Eds.).
23. Gerfen C.R., Baimbridge K.G., Miller J.J. The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:8780-8784.
24. Handforth A., DeSalles A.A., Krahl S.E. Deep brain stimulation of the subthalamic nucleus as adjunct treatment for refractory epilepsy. Epilepsia 2006, 47:1239-1241.
25. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Prog. Neurobiol. 1996, 50:83-107.
26. Iadarola M.J., Gale K. Substantia nigra: site of anticonvulsant activity mediated by gamma-aminobutyric acid. Science 1982, 218:1237-1240.
27. Kahane P., Depaulis A. Deep brain stimulation in epilepsy: what is next?. Curr. Opin. Neurol. 2010, 23:177-182.
28. 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, 45:346-354.
29. Kringelbach M.L., Jenkinson N., Owen S.L., Aziz T.Z. Translational principles of deep brain stimulation. Nat. Rev. Neurosci. 2007, 8:623-635.
30. Kwan P., Brodie M.J. Epilepsy after the first drug fails: substitution or add-on?. Seizure 2000, 9:464-468.
31. Kwan P., Brodie M.J. Drug treatment of epilepsy: when does it fail and how to optimize its use?. CNS Spectr. 2004, 9:110-119.
32. Lado F.A., Velisek L., Moshe S.L. The effect of electrical stimulation of the subthalamic nucleus on seizures is frequency dependent. Epilepsia 2003, 44:157-164.
33. Lockman J., Fisher R.S. Therapeutic brain stimulation for epilepsy. Neurol. Clin. 2009, 27:1031-1040.
34. Loddenkemper T., Pan A., Neme S., Baker K.B., Rezai A.R., Dinner D.S., Montgomery E.B., Luders H.O. Deep brain stimulation in epilepsy. J. Clin. Neurophysiol. 2001, 18:514-532.
35. Löscher W., Nolting B. The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. IV. Protective indices. Epilepsy Res. 1991, 9:1-10.
36. Löscher W., Schmidt D. New Horizons in the development of antiepileptic drugs: innovative strategies. Epilepsy Res. 2006, 69:183-272.
37. Luckman S.M., Dyball R.E., Leng G. Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. J. Neurosci. 1994, 14:4825-4830.
38. McIntyre C.C., Savasta M., Kerkerian-Le G.L., Vitek J.L. Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin. Neurophysiol. 2004, 115:1239-1248.
39. McIntyre C.C., Savasta M., Walter B.L., Vitek J.L. How does deep brain stimulation work? Present understanding and future questions. J. Clin. Neurophysiol. 2004, 21:40-50.
40. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 1991, 14:421-451.
41. Morgan J.I., Cohen D.R., Hempstead J.L., Curran T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 1987, 237:192-197.
42. Morimoto K., Goddard G.V. The substantia nigra is an important site for the containment of seizure generalization in the kindling model of epilepsy. Epilepsia 1987, 28:1-10.
43. Moshé S.L., Brown L.L., Kubová H., Velísková J., Zukin R.S., Sperber E.F. Maturation and segregation of brain networks that modify seizures. Brain Res. 1994, 665:141-146.
44. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
45. Nagel S., Najm I.M. Deep brain stimulation for epilepsy. Neuromodulation Technol. Neural Interface 2009, 12:270-279.
46. Paxinos P., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego.
47. Ruskin D.N., Marshall J.F. D1 dopamine receptors influence Fos immunoreactivity in the globus pallidus and subthalamic nucleus of intact and nigrostriatal-lesioned rats. Brain Res. 1995, 703:156-164.
48. Saillet S., Langlois M., Feddersen B., Minotti L., Vercueil L., Chabardes S., David O., Depaulis A., Deransart C., Kahane P. Manipulating the epileptic brain using stimulation: a review of experimental and clinical studies. Epileptic Disord. 2009, 11:100-112.
49. Shehab S.A., Julyan T.E. Induction of Fos-like immunoreactivity in the basal ganglia by ether anaesthesia: effects of injections of muscimol in rostral versus caudal substantia nigra pars reticulata. Exp. Brain Res. 2002, 142:227-240.
50. Shehab S., Coffey P., Dean P., Redgrave P. Regional expression of fos-like immunoreactivity following seizures induced by pentylenetetrazole and maximal electroshock. Exp. Neurol. 1992, 118:261-274.
51. Shehab S., Simkins M., Dean P., Redgrave P. The dorsal midbrain anticonvulsant zone-I: effects of locally administered excitatory amino acids or bicuculline on maximal electroshock seizures. Neuroscience 1995, 65:671-679.
52. Shehab S., Simkins M., Dean P., Redgrave P. The dorsal midbrain anticonvulsant zone-III. Effects of efferent pathway transections on suppression of electroshock seizures and defence-like reactions produced by local injections of bicuculline. Neuroscience 1995, 65:697-708.
53. Shehab S., Simkins M., Dean P., Redgrave P. Regional distribution of the anticonvulsant and behavioural effects of muscimol injected into the substantia nigra of rats. Eur. J. Neurosci. 1996, 8:749-757.
54. Shehab S., Guadagno J., Ferguson K., Redgrave P. Regional distribution of the anticonvulsant and behavioural effects of bicuculline injected into the pontine reticular formation of rats. Eur. J. Neurosci. 1997, 9:1875-1884.
55. Shehab S.A., Ljubisavljevic M., Al Halhali F., Al Awadhi A., Madathil M., Abdul-Kareem A., Redgrave P. Experimental manipulations of the subthalamic nucleus fail to suppress tonic seizures in the electroshock model of epilepsy. Exp. Brain Res. 2006, 173:274-281.
56. Shehab S., Alzigali L., Madathil M., Redgrave P. Pharmacological evidence for an anticonvulsant relay in the rat ventromedial medulla. Eur. J. Neurosci. 2007, 26:2585-2594.
57. Shehab S.A., Al-Nahdi A., Al-Zaabi F., Al-Mugaddam F., Al-Sultan M., Ljubisavljevic M. Does Deep Brain Stimulation of Substantia Nigra Suppress Tonic Epileptic Seizures?. 16th World Congress on Basic and Clinical Pharmacology-Copenhagen, Denmark 2010, 3549.
58. Shi L.H., Luo F., Woodward D., Chang J.Y. Deep brain stimulation of the substantia nigra pars reticulata exerts long lasting suppression of amygdala-kindled seizures. Brain Res. 2006, 1090:202-207.
59. Sonnenberg J.L., Macgregor-Leon P.F., Curran T., Morgan J.I. Dynamic alterations occur in the levels and composition of transcription factor AP-1 complexes after seizure. Neuron 1989, 3:359-365.
60. Swinyard E.A. Electrically induced convulsions. Experimental Models of Epilepsy-Manual for Laboratory Worker 1972, 433-458. Raven Press, New York. D.P. Purpura, D.M. Woodbury, D.B. Tower, R.D. Walter, J.K. Penry (Eds.).
61. Theodore W.H., Fisher R.S. Brain stimulation for epilepsy. Lancet Neurol. 2004, 3:111-118.
62. Usui N., Maesawa S., Kajita Y., Endo O., Takebayashi S., Yoshida J. Suppression of secondary generalization of limbic seizures by stimulation of subthalamic nucleus in rats. J. Neurosurg. 2005, 102:1122-1129.
63. Velisek L., Velísková J., Moshé S.L. Electrical stimulation of substantia nigra pars reticulata is anticonvulsant in adult and young male rats. Exp. Neurol. 2002, 173:145-152.
64. Velísková J., Velsek L., Moshé S.L. Subthalamic nucleus: a new anticonvulsant site in the brain. Neuroreport 1996, 7:1786-1788.
65. Velísková J., Löscher W., Moshé S.L. Regional and age specific effects of zolpidem microinfusions in the substantia nigra on seizures. Epilepsy Res. 1998, 30:107-114.
66. Vercueil L., Benazzouz A., Deransart C., Bressand K., Marescaux C., Depaulis A., Benabid A.L. High-frequency stimulation of the subthalamic nucleus suppresses absence seizures in the rat: comparison with neurotoxic lesions. Epilepsy Res. 1998, 31:39-46.
67. Vitek J.L. Mechanisms of deep brain stimulation: excitation or inhibition. Mov. Disord. 2002, 17(Suppl. 3):S69-S72.
68. Wille C., Steinhoff B.J., Altenmüller D.M., Staack A.M., Bilic S., Nikkhah G., Vesper J. Chronic high-frequency deep-brain stimulation in progressive myoclonic epilepsy in adulthood-report of five cases. Epilepsia 2011, 52:489-496.
69. Wirtshafter D., Asin K.E. Dopamine antagonists induce fos-like-immunoreactivity in the substantia nigra and entopeduncular nucleus of the rat. Brain Res. 1995, 670:205-214.