The anticonvulsant response to valproate in kindled rats is correlated with its effect on neuronal firing in the substantia nigra pars reticulata: A new mechanism of pharmacoresistance

Journal of Neuroscience

Volumn 31, Issue 45, 2011, Pages 16423-16434

  Töllner, Kathrin ^a,b   Wolf, Saskia ^a   Löscher, Wolfgang ^a,b   Gernert, Manuela ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VALPROIC ACID;

AFTERDISCHARGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ANTICONVULSANT RESPONSE; ARTICLE; ATAXIA; BODY TEMPERATURE; CONTROLLED STUDY; DISEASE DURATION; DISEASE SEVERITY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG RESPONSE; FEMALE; HYPOLOCOMOTION; KINDLING; LOCOMOTION; MOTOR COORDINATION; MUSCLE RELAXATION; NONHUMAN; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; ROTAROD TEST; SEDATION; SEIZURE; SEIZURE THRESHOLD; SPIKE WAVE; SUBSTANTIA NIGRA PARS RETICULATA;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANTICONVULSANTS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ELECTRODES; FEMALE; KINDLING, NEUROLOGIC; NEURONS; RATS; RATS, WISTAR; SEIZURES; STATISTICS AS TOPIC; SUBSTANTIA NIGRA; VALPROIC ACID;

EID: 80755143545     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2506-11.2011     Document Type: Article

References (55)

1. Albala BJ, Moshé SL, Okada R (1984) Kainic-acid-induced seizures: a developmental study. Brain Res 315:139-148.
2. Deniau JM, Hammond C, Riszk A, Feger J (1978) Electrophysiological properties of identified output neurons of the rat substantia nigra (pars compacta and pars reticulata): evidences for the existence of branched neurons. Exp Brain Res 32:409-422.
3. Depaulis A, Vergnes M, Marescaux C (1994) Endogenous control of epilepsy: the nigral inhibitory system. Prog Neurobiol 42:33-52.
4. De Sarro G, Meldrum BS, Reavill C (1984) Anticonvulsant action of 2-amino-7-phosphonoheptanoic acid in the substantia nigra. Eur J Pharmacol 106:175-179.
5. De Sarro G, Patel S, Meldrum BS (1986) Anticonvulsant action of a kainate antagonist gamma-D-glutamyl aminomethylsulphonic acid injected focally into the substantia nigra and entopeduncular nucleus. Eur J Pharmacol 132:229-236.
6. De Sarro G, De Sarro A, Meldrum BS (1991) Anticonvulsant action of 2-chloroadenosine injected focally into the inferior colliculus and substantia nigra. Eur J Pharmacol 194:145-152.
7. Dickinson RG, Harland RC, Ilias AM, Rodgers RM, Kaufman SN, Lynn RK, Gerber N (1979) Disposition of valproic acid in the rat: dose-dependent metabolism, distribution, enterohepatic recirculation and choleretic effect. J Pharmacol Exp Ther 211:583-595.
8. Ebert U, Löscher W (1999) Characterization of phenytoin-resistant kindled rats, a new model of drug-resistant partial epilepsy: influence of genetic factors. Epilepsy Res 33:217-226.
9. Ebert U, Rundfeldt C, Lehmann H, Löscher W (1999) Characterization of phenytoin-resistant kindled rats, a new model of drug-resistant partial epilepsy: influence of experimental and environmental factors. Epilepsy Res 33:199-215.
10. Farrant M, Webster RA (1989) Neuronal activity, amino acid concentration and amino acid release in the substantia nigra of the rat after sodium valproate. Brain Res 504:49-56.
11. Freichel C, Ebert U, Potschka H, Löscher W (2004) Amygdala-kindling does not induce a persistent loss of GABA neurons in the substantia nigra pars reticulata of rats. Brain Res 1025:203-209.
12. French JA (2007) Refractory epilepsy: clinical overview. Epilepsia 48 [Suppl 1]:3-7.
13. A receptor function in rat substantia nigra. Exp Neurol 183:628-637.
14. Gale K, Proctor M, Velísková J, Nehlig A (2008) Basal ganglia and brainstem anatomy and physiology. In: Epilepsy: a comprehensive textbook (Engel JJ, Pedley TA, eds), pp 367-384. Philadelphia: Lippincott Williams and Wilkins.
15. Garcia-Cairasco N, Sabbatini RM (1983) Role of the substantia nigra in audiogenic seizures: a neuroethological analysis in the rat. Braz J Med Biol Res 16:171-183.
16. Gernert M, Löscher W (2001) Lack of robust anticonvulsant effects of muscimol microinfusions in the anterior substantia nigra of kindled rats. Eur J Pharmacol 432:35-41.
17. Gernert M, Fedrowitz M, Wlaz P, Löscher W (2004) Subregional changes in discharge rate, pattern, and drug sensitivity of putative GABAergic nigral neurons in the kindling model of epilepsy. Eur J Neurosci 20:2377-2386.
18. Grace AA, Bunney BS (1979) Paradoxical GABA excitation of nigral dopaminergic cells: indirect mediation through reticulata inhibitory neurons. Eur J Pharmacol 59:211-218.
19. Guyenet PG, Aghajanian GK (1978) Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra. Brain Res 150:69-84.
20. Iadarola MJ, Gale K (1982) Substantia nigra: site of anticonvulsant activity mediated by gamma-aminobutyric acid. Science 218:1237-1240.
21. Kaneoke Y, Vitek JL (1996) Burst and oscillation as disparate neuronal properties. J Neurosci Methods 68:211-223.
22. Kerwin RW, Olpe HR, Schmutz M (1980) The effect of sodium-n-dipropyl acetate on gamma-aminobutyric acid-dependent inhibition in the rat cortex and substantia nigra in relation to its anticonvulsant activity. Br J Pharmacol 71:545-551.
23. Kücker S, Töllner K, Piechotta M, Gernert M (2010) Kindling as a model of temporal lobe epilepsy induces bilateral changes in spontaneous striatal activity. Neurobiol Dis 37:661-672.
24. Le Gal La Salle G, Kaijima M, Feldblum S (1983) Abortive amygdaloid kindled seizures following microinjection of gamma-vinyl-GABA in the vicinity of substantia nigra in rats. Neurosci Lett 36:69-74.
25. Löscher W (1989) Valproate enhances GABA turnover in the substantia nigra. Brain Res 501:198-203.
26. Löscher W (2002) Basic pharmacology of valproate: a review after 35 years of clinical use for the treatment of epilepsy. CNS Drugs 16:669-694.
27. Löscher W (2006) Animal models of drug-refractory epilepsy. In: Models of seizures and epilepsy (Pitkänen A, Schwartzkroin PA, Moshe SL, eds), pp 551-567. Burlington, MA: Academic.
28. Löscher W (2007) The pharmacokinetics of antiepileptic drugs in rats: consequences for maintaining effective drug levels during prolonged drug administration in rat models of epilepsy. Epilepsia 48:1245-1258.
29. Löscher W, Potschka H (2005) Drug resistance in brain diseases and the role of drug efflux transporters. Nat Rev Neurosci 6:591-602.
30. Löscher W, Rundfeldt C (1991) Kindling as a model of drug-resistant partial epilepsy: selection of phenytoin-resistant and nonresistant rats. J Pharmacol Exp Ther 258:483-489.
31. Löscher W, Schwark WS (1985) Evidence for impaired GABAergic activity in the substantia nigra of amygdaloid kindled rats. Brain Res 339: 146-150.
32. Löscher W, Schwark WS (1987) Further evidence for abnormal GABAergic circuits in amygdala-kindled rats. Brain Res 420:385-390.
33. Löscher W, Rundfeldt C, Hönack D (1993) Pharmacological characterization of phenytoin-resistant amygdala-kindled rats, a new model of drugresistant partial epilepsy. Epilepsy Res 15:207-219.
34. Löscher W, Rohlfs A, Rundfeldt C (1995) Reduction in firing rate of substantia nigra pars reticulata neurons by valproate: influence of different types of anesthesia in rats. Brain Res 702:133-144.
35. McNamara JO, Galloway MT, Rigsbee LC, Shin C (1984) Evidence implicating substantia nigra in regulation of kindled seizure threshold. J Neurosci 4:2410-2417.
36. Moshé SL, Albala BJ (1984) Nigral muscimol infusions facilitate the development of seizures in immature rats. Brain Res 315:305-308.
37. Moshé SL, Sperber EF, Brown LL, Tempel A (1992) Age-dependent changes in substantia nigra GABA-mediated seizure suppression. Epilepsy Res Suppl 8:97-106.
38. Moshé SL, Brown LL, Kubová H, Velísková J, Zukin RS, Sperber EF (1994) Maturation and segregation of brain networks that modify seizures. Brain Res 665:141-146.
39. Moshé SL, Garant DS, Sperber EF, Velísková J, Kubova H, Brown LL (1995) Ontogeny and topography of seizure regulation by the substantia nigra. Brain Dev 17 [Suppl]:61-72.
40. Nolte MW, Löscher W, Gernert M (2006) Pedunculopontine neurons are involved in network changes in the kindling model of temporal lobe epilepsy. Neurobiol Dis 23:206-218.
41. Paxinos G, Watson C (2007) The rat brain in stereotactic coordinates, Ed 6. Amsterdam: Academic.
42. Potschka H, Löscher W (2001) In vivo evidence for P-glycoproteinmediated transport of phenytoin at the blood-brain barrier of rats. Epilepsia 42:1231-1240.
43. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
44. Remy S, Beck H (2006) Molecular and cellular mechanisms of pharmacoresistance in epilepsy. Brain 129:18-35.
45. Rohlfs A, Rundfeldt C, Koch R, Löscher W (1996) A comparison of the effects of valproate and its major active metabolite E-2-en-valproate on single unit activity of substantia nigra pars reticulata neurons in rats. J Pharmacol Exp Ther 277:1305-1314.
46. Rundfeldt C, Hönack D, Löscher W (1990) Phenytoin potently increases the threshold for focal seizures in amygdala-kindled rats. Neuropharmacology 29:845-851.
47. Schmidt D, Löscher W (2005) Drug resistance in epilepsy: putative neurobiologic and clinical mechanisms. Epilepsia 46:858-877.
48. Simons DJ, Land PW (1987) A reliable technique for marking the location of extracellular recording sites using glass micropipettes. Neurosci Lett 81:100-104.
49. Sperber EF, Wong BY, Wurpel JN, Moshé SL (1987) Nigral infusions of muscimol or bicuculline facilitate seizures in developing rats. Brain Res 465:243-250.
50. Szoeke CE, Newton M, Wood JM, Goldstein D, Berkovic SF, O'Brien TJ, Sheffield LJ (2006) Update on pharmacogenetics in epilepsy: a brief review. Lancet Neurol 5:189-196.
51. 14C]2-deoxyglucose mapping in rats: possible implications for autistic repetitive behaviors. Neurobiol Dis 18:346-355.
52. Velísková J, Löscher W, Moshé SL (1998) Regional and age specific effects of zolpidem microinfusions in the substantia nigra on seizures. Epilepsy Res 30:107-114.
53. Velísková J, Liptáková S, Hussain S (2001) The effects of N-methyl-D-aspartate antagonist 2-amino-7-phosphonoheptanoic acid microinfusions into the adult male rat substantia nigra pars reticulata are site-specific. Neurosci Lett 316:108-110.
54. Wahnschaffe U, Löscher W (1992) Lack of changes in seizure susceptibility during the estrous cycle in kindled rats. Epilepsy Res 13:199-204.
55. Waszczak BL, Lee EK, Walters JR (1986) Effects of anticonvulsant drugs on substantia nigra pars reticulata neurons. J Pharmacol Exp Ther 239:606-611.