Vigabatrin for focal drug delivery in epilepsy: Bilateral microinfusion into the subthalamic nucleus is more effective than intranigral or systemic administration in a rat seizure model

Neurobiology of Disease

Volumn 46, Issue 2, 2012, Pages 362-376

  Bröer, Sonja ^a   Backofen Wehrhahn, Bianca ^a   Bankstahl, Marion ^a   Gey, Laura ^a   Gernert, Manuela ^a   Löscher, Wolfgang ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Basal ganglia; Blood brain barrier; GABA; Pentylenetetrazole; Substantia nigra

Indexed keywords

PENTETRAZOLE; VIGABATRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; DRUG SPECIFICITY; ENTOPEDUNCULAR NUCLEUS; EPILEPSY; ESTRUS CYCLE; FEMALE; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE THRESHOLD; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; EPILEPSY; FEMALE; MICROINJECTIONS; RATS; RATS, WISTAR; SEIZURES; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS; TREATMENT OUTCOME; VIGABATRIN;

EID: 84859488867     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.01.017     Document Type: Article

References (83)

1. Al-Otaibi F.A., Hamani C., Lozano A.M. Neuromodulation in epilepsy. Neurosurgery 2011, 69:957-979.
2. Bähner F., Weiss E.K., Birke G., Maier N., Schmitz D., Rudolph U., Frotscher M., Traub R.D., Both M., Draguhn A. Cellular correlate of assembly formation in oscillating hippocampal networks in vitro. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:E607-E616.
3. Benabid A.L., Koudsie A., Pollak P., Kahane P., Chabardes S., Hirsch E., Marescaux C., Benazzouz A. Future prospects of brain stimulation. Neurol. Res. 2000, 22:237-246.
4. Brodie M.J. Antiepileptic drug therapy the story so far. Seizure 2010, 19:650-655.
5. Casu M., Gale K. Intracerebral injection of gamma vinyl GABA: method for measuring rates of GABA synthesis in specific brain regions in vivo. Life Sci. 1981, 29:681-688.
6. Deniau J.M., Mailly P., Maurice N., Charpier S. The pars reticulata of the substantia nigra: a window to basal ganglia output. Prog. Brain Res. 2007, 160:151-172.
7. Depaulis A., Vergnes M., Marescaux C. Endogenous control of epilepsy: the nigral inhibitory system. Prog. Neurobiol. 1994, 42:33-52.
8. 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.
9. 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.
10. Duncan J.S. Epilepsy in 2010: refinement of optimal medical and surgical treatments. Nat. Rev. Neurol. 2011, 7:72-74.
11. Dybdal D., Gale K. Postural and anticonvulsant effects of inhibition of the rat subthalamic nucleus. J. Neurosci. 2000, 20:6728-6733.
12. Dybdal D., Dubach M., Vaurio R., Estabrooke I., Heath A., Gale K. Focal inhibition of primate substantia nigra is anticonvulsant. Epilepsia 1997, 38(Suppl. 8):18.
13. Everett J.W. Neurobiology of reproduction in the female rat. A fifty-year perspective. Monogr. Endocrinol. 1989, 32:1-133.
14. Faingold C.L., Fromm G.H. Drugs for Control of Epilepsy: Actions on Neuronal Networks Involved in Seizure Disorders 1992, CRC Press, Boca Raton.
15. Finn D.A., Gee K.W. The estrus cycle, sensitivity to convulsants and the anticonvulsant effect of a neuroactive steroid. J. Pharmacol. Exp. Ther. 1994, 271:164-170.
16. Fisher R.S., Ho J. Potential new methods for antiepileptic drug delivery. CNS Drugs 2002, 16:579-593.
17. Gale K. Mechanisms of seizure control mediated by g-aminobutyric acid: role of the substantia nigra. Fed. Proc. 1985, 44:2414-2424.
18. Gale K. Progression and generalization of seizure discharge: anatomical and neurochemical substrates. Epilepsia 1988, 29(Suppl.2):S15-S34.
19. Gale K. GABA and epilepsy: basic concepts from preclinical research. Epilepsia 1992, 33(Suppl. 5):S3-S12.
20. Gale K. Subcortical structures and pathways involved in convulsive seizure generation. J. Clin. Neurophysiol. 1992, 9:264-277.
21. Gale K., Iadarola M.J. Seizure protection and increased nerve-terminal GABA: delayed effects of GABA transaminase inhibition. Science 1980, 208:288-291.
22. Gale K., Proctor M., Veliskova J., Nehlig A. Basal ganglia and brainstem anatomy and physiology. Epilepsy. A Comprehensive Textbook 2008, 367-384. Lippincott Williams & Wilkins, Philadelphia. Second edition. J.J. Engel, T.A. Pedley (Eds.).
23. Gernert M., Löscher W. Lack of robust anticonvulsant effects of muscimol microinfusions in the anterior substantia nigra of kindled rats. Eur. J. Pharmacol. 2001, 432:35-41.
24. Gernert M., Fedrowitz M., Wlaz P., Löscher W. Subregional changes in discharge rate, pattern, and drug sensitivity of putative GABAergic nigral neurons in the kindling model of epilepsy. Eur. J. Neurosci. 2004, 20:2377-2386.
25. Hamani C., Saint-Cyr J.A., Fraser J., Kaplitt M., Lozano A.M. The subthalamic nucleus in the context of movement disorders. Brain 2004, 127:4-20.
26. Hammond E.J., Wilder B.J. Gamma-vinyl GABA: a new antiepileptic drug. Clin. Neuropharmacol. 1985, 8:1-12.
27. Hardman C.D., Henderson J.M., Finkelstein D.I., Horne M.K., Paxinos G., Halliday G.M. Comparison of the basal ganglia in rats, marmosets, macaques, baboons, and humans: volume and neuronal number for the output, internal relay, and striatal modulating nuclei. J. Comp. Neurol. 2002, 445:238-255.
28. Haugvicova R., Kubova H., Mares P. Does vigabatrin possess an anticonvulsant action against pentylenetetrazol-induced seizures in developing rats?. Physiol. Res. 2002, 51:363-370.
29. Heiss J.D., Walbridge S., Morrison P., Hampton R.R., Sato S., Vortmeyer A., Butman J.A., O'Malley J., Vidwan P., Dedrick R.L., Oldfield E.H. Local distribution and toxicity of prolonged hippocampal infusion of muscimol. J. Neurosurg. 2005, 103:1035-1045.
30. Heiss J.D., Walbridge S., Asthagiri A.R., Lonser R.R. Image-guided convection-enhanced delivery of muscimol to the primate brain. J. Neurosurg. 2010, 112:790-795.
31. Holland K.D., McKeon A.C., Canney D.J., Covey D.F., Ferrendelli J.A. Relative anticonvulsant effects of GABAmimetic and GABA modulatory agents. Epilepsia 1992, 33:981-986.
32. Hönack D., Löscher W. Kindling increases the sensitivity of rats to adverse effects of certain antiepileptic drugs. Epilepsia 1995, 36:763-771.
33. Iadarola M.J., Gale K. Cellular compartments of GABA in brain and their relationship to anticonvulsant activity. Mol. Cell. Biochem. 1981, 39:305-330.
34. Iadarola M.J., Gale K. Substantia nigra: site of anticonvulsant activity mediated by g-aminobutyric acid. Science 1982, 218:1237-1240.
35. Jung M.J., Lippert B., Metcalf B.W., Bohlen P., Schechter P.J. gamma-Vinyl GABA (4-amino-hex-5-enoic acid), a new selective irreversible inhibitor of GABA-T: effects on brain GABA metabolism in mice. J. Neurochem. 1977, 29:797-802.
36. Kahane P., Depaulis A. Deep brain stimulation in epilepsy: what is next?. Curr. Opin. Neurol. 2010, 23:177-182.
37. Kücker S., Töllner K., Piechotta M., Gernert M. Kindling as a model of temporal lobe epilepsy induces bilateral changes in spontaneous striatal activity. Neurobiol. Dis. 2010, 37:661-672.
38. Le Gal La Salle G., Kaijima M., Feldblum S. Abortive amygdaloid kindled seizures following microinjection of gamma-vinyl-GABA in the vicinity of substantia nigra in rats. Neurosci. Lett. 1983, 36:69-74.
39. Le Gal La Salle G., Kaijima M., Feldblum S. Nigral GABAergic mechanisms in the control of kindled seizure development in the rat. Current Problems in Epilepsy. Cerebral Blood Flow, Metabolism and Epilepsy 1983, 365-369. John Libbey, London. M. Baldy-Moulinier, D.-H. Ingvar, B.S. Meldrum (Eds.).
40. Lega B.C., Halpern C.H., Jaggi J.L., Baltuch G.H. Deep brain stimulation in the treatment of refractory epilepsy: update on current data and future directions. Neurobiol. Dis. 2010, 38:354-360.
41. Löscher W. A comparative study of the pharmacology of inhibitors of GABA-metabolism. Naunyn Schmiedebergs Arch. Pharmacol. 1980, 315:119-128.
42. Löscher W. Relationship between drug-induced changes in seizure thresholds and the GABA content of brain and brain nerve endings. Naunyn Schmiedebergs Arch. Pharmacol. 1981, 317:131-134.
43. Löscher W. Comparative assay of anticonvulsant and toxic potencies of sixteen GABAmimetic drugs. Neuropharmacology 1982, 21:803-810.
44. Löscher W. Preclinical assessment of proconvulsant drug activity and its relevance for predicting adverse events in humans. Eur. J. Pharmacol. 2009, 610:1-11.
45. Löscher W., Ebert U. Basic mechanisms of seizure propagation: targets for rational drug design and rational polypharmacy. Epilepsy Res. Suppl. 1996, 11:17-44.
46. Löscher W., Hörstermann D. Differential effects of vigabatrin, gamma-acetylenic GABA, aminooxyacetic acid, and valproate on levels of various amino acids in rat brain regions and plasma. Naunyn Schmiedebergs Arch. Pharmacol. 1994, 349:270-278.
47. Löscher W., Potschka H. Drug resistance in brain diseases and the role of drug efflux transporters. Nat. Rev. Neurosci. 2005, 6:591-602.
48. Löscher W., Schmidt D. Which animal models should be used in the search for new antiepileptic drugs? A proposal based on experimental and clinical considerations. Epilepsy Res. 1988, 2:145-181.
49. Löscher W., Schmidt D. Modern antiepileptic drug development has failed to deliver: ways out of the current dilemma. Epilepsia 2011, 52:657-678.
50. Löscher W., Czuczwar S., Jäckel R., Schwarz M. Effect of microinjections of g-vinyl GABA or isoniazid into substantia nigra on the development of amygdala kindling in rats. Exp. Neurol. 1987, 95:622-638.
51. Löscher W., Hönack D., Gramer M. Use of inhibitors of gamma-aminobutyric acid (GABA) transaminase for the estimation of GABA turnover in various brain regions of rats: a reevaluation of aminooxyacetic acid. J. Neurochem. 1989, 53:1737-1750.
52. Löscher W., Jäckel R., Müller F. Anticonvulsant and proconvulsant effects of inhibitors of GABA degradation in the amygdala-kindling model. Eur. J. Pharmacol. 1989, 163:1-14.
53. Löscher W., Hönack D., Fassbender C.P., Nolting B. The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. III. Pentylenetetrazol seizure models. Epilepsy Res. 1991, 8:171-189.
54. Löscher W., Cole A.J., Mclean M.J. Commentary: physical approaches for the treatment of epilepsy: electrical and magnetic stimulation and cooling. Neurotherapeutics 2009, 6:258-262.
55. Luszczki J.J., Ratnaraj N., Patsalos P.N., Czuczwar S.J. Isobolographic and behavioral characterizations of interactions between vigabatrin and gabapentin in two experimental models of epilepsy. Eur. J. Pharmacol. 2008, 595:13-21.
56. McNamara J.O., Galloway M.T., Rigsbee L.C., Shin C. Evidence implicating substantia nigra in regulation of kindled seizure threshold. J. Neurosci. 1984, 4:2410-2417.
57. Miller J.W., McKeon A.C., Ferrendelli J.A. Functional anatomy of pentylenetetrazol and electroshock seizures in the rat brainstem. Ann. Neurol. 1987, 22:615-621.
58. Mohanraj R., Brodie M.J. Pharmacological outcomes in newly diagnosed epilepsy. Epilepsy Behav. 2005, 6:382-387.
59. Moshé S.L., Brown L.L., Kubova H., Veliskova J., Zukin R.S., Sperber E.F. Maturation and segregation of brain networks that modify seizures. Brain Res. 1994, 665:141-146.
60. Moshé S.L., Garant D.S., Sperber E.F., Veliskova J., Kubova H., Brown L.L. Ontogeny and topography of seizure regulation by the substantia nigra. Brain Dev. 1995, 17(Suppl):61-72.
61. Myslobodsky M.S., Ackermann R.F., Engel J. Effects of gamma-acetylenic GABA and gamma-vinyl GABA on metrazol-activated, and kindled seizures. Pharmacol. Biochem. Behav. 1979, 11:265-271.
62. Nilsen K.E., Cock H.R. Focal treatment for refractory epilepsy: hope for the future?. Brain Res. Brain Res. Rev. 2004, 44:141-153.
63. Nolte M.W., Heile A., Gernert M. Microinfusions of gamma-vinyl GABA but not muscimol into the anterior substantia nigra pars reticulata exerts robust anticonvulsant effects in male kindled rats. Abstracts from the 7th European Congress on Epileptology, Helsinki, Finland, 2nd-6th July 2006 2006, 312.
64. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Elsevier, Amsterdam. 6th ed.
65. Potschka H., Löscher W., Wlaz P., Behl B., Hofmann H.P., Treiber H.-J., Szabo L. LU 73068, a new non-NMDA and glycine/NMDA receptor antagonist: pharmacological characterization and comparison with NBQX and L-701,324 in the kindling model of epilepsy. Br. J. Pharmacol. 1998, 125:1258-1266.
66. Rattka M., Brandt C., Bankstahl M., Bröer S., Löscher W. Enhanced susceptibility to the GABA antagonist pentylenetetrazole during the latent period following a pilocarpine-induced status epilepticus in rats. Neuropharmacology 2011, 60:505-512.
67. Rogawski M.A. Convection-enhanced delivery in the treatment of epilepsy. Neurotherapeutics 2009, 6:344-351.
68. Sabers A., Gram L. Pharmacology of vigabatrin. Pharmacol. Toxicol. 1992, 70:237-243.
69. Sayin U., Cengiz S., Altug T. Vigabatrin as an anticonvulsant against pentylenetetrazol seizures. Pharmacol. Res. 1993, 28:325-331.
70. Schwabe K., Ebert U., Löscher W. Bilateral microinjections of vigabatrin in the central piriform cortex retard amygdala kindling in rats. Neuroscience 2004, 129:425-429.
71. 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.
72. Shin C., Rigsbee L.C., McNamara J.O. Anti-seizure and anti-epileptogenic effect of gamma-vinyl gamma-aminobutyric acid in amygdaloid kindling. Brain Res. 1986, 398:370-374.
73. Shorr E. A new technic for staining vaginal smears: III. A single differential stain. Science 1941, 94:545-546.
74. Shorvon S.D. Drug treatment of epilepsy in the century of the ILAE: the second 50 years, 1959-2009. Epilepsia 2009, 50(Suppl 3):93-130.
75. Sills G.J., Butler E., Forrest G., Ratnaraj N., Patsalos P.N., Brodie M.J. Vigabatrin, but not gabapentin or topiramate, produces concentration-related effects on enzymes and intermediates of the GABA shunt in rat brain and retina. Epilepsia 2003, 44:886-892.
76. Smolders I., Khan G.M., Lindekens H., Prikken S., Marvin C.A., Manil J., Ebinger G., Michotte Y. Effectiveness of vigabatrin against focally evoked pilocarpine-induced seizures and concomitant changes in extracellular hippocampal and cerebellar glutamate, gamma-aminobutyric acid and dopamine levels, a microdialysis-electrocorticography study in freely moving rats. J. Pharmacol. Exp. Ther. 1997, 283:1239-1248.
77. Theodore W.H., Fisher R. Brain stimulation for epilepsy. Acta Neurochir. Suppl. 2007, 97:261-272.
78. Tong X., Ratnaraj N., Patsalos P.N. Vigabatrin extracellular pharmacokinetics and concurrent gamma-aminobutyric acid neurotransmitter effects in rat frontal cortex and hippocampus using microdialysis. Epilepsia 2009, 50:174-183.
79. Turski L., Cavalheiro E.A., Schwarz M., Turski W.A., Moraes Mello L.E., Bortolotto Z.A., Klockgether T., Sontag K.H. Susceptibility to seizures produced by pilocarpine in rats after microinjection of isoniazid or gamma-vinyl-GABA into the substantia nigra. Brain Res. 1986, 370:294-309.
80. Veliskova J., Velsek L., Moshé S.L. Subthalamic nucleus: a new anticonvulsant site in the brain. Neuroreport 1996, 7:1786-1788.
81. Veliskova 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.
82. Willmore L.J., Abelson M.B., Ben Menachem E., Pellock J.M., Shields W.D. Vigabatrin: 2008 update. Epilepsia 2009, 50:163-173.
83. Xu S.G., Garant D.S., Sperber E.F., Moshé S.L. Effects of substantia nigra gamma-vinyl-GABA infusions on flurothyl seizures in adult rats. Brain Res. 1991, 566:108-114.