Progressive metabolic changes underlying the chronic reorganization of brain circuits during the silent phase of the lithium-pilocarpine model of epilepsy in the immature and adult rat

Experimental Neurology

Volumn 162, Issue 1, 2000, Pages 146-157

  Dubé, Céline ^a   Boyet, Sylvette ^a   Marescaux, Christian ^a   Nehlig, Astrid ^a  

^a INSERM   (France)

Author keywords

2 14C deoxyglucose; Cerebral glucose metabolism; Epilepsy; Lithium pilocarpine; Neuronal damage; Postnatal development; Seizures; Silent period

Indexed keywords

CARBON 14; DEOXYGLUCOSE; GLUCOSE; LITHIUM; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN METABOLISM; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; FEMALE; GLUCOSE METABOLISM; MALE; METABOLIC RATE; NERVE CELL DEGENERATION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SEIZURE;

EID: 0034024591     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.2000.7324     Document Type: Article

References (48)

1. Alexander G., Crutcher M. Functional architecture of basal ganglia circuits: Neural substrates of parallel processing. Trends Neurosci. 13:1990;266-271.
2. Bevan M. D., Smith A. D., Bolam J. P. The substantia nigra as a site of synaptic integration of functionally diverse information arising from the ventral pallidum and the globus pallidus in the rat. Neuroscience. 75:1996;5-12.
3. Bonhaus D. W., Russell R. D., McNamara J. O. Activation of substantia nigra pars reticulata neurons: Role in the initiation and behavioral expression of kindled seizures. Brain Res. 545:1991;41-48.
4. Calabresi P., De Murtas M., Bernardi G. The neostriatum beyond the motor function: Experimental and clinical evidence. Neuroscience. 78:1997;39-60.
5. Camfield P., Camfield C., Gordon K., Dooley J. What types of epilepsy are preceded by febrile seizures? A population-based study of children. Dev. Med. Child Neurol. 36:1994;887-892.
6. Cavalheiro E. A. The pilocarpine model of epilepsy. Ital. J. Neurol. Sci. 16:1995;33-37.
7. Cavalheiro E. A., Silva D. F., Turski W. A., Calderazzo-Filho L. S., Bortolotto A., Turski L. The susceptibility of rats to pilocarpine-induced seizures is age-dependent. Dev. Brain Res. 37:1987;43-58.
8. Cavalheiro E. A., Turski L. Intrastriatal N-methyl-d-aspartate prevents amygdala kindled seizures in rats. Brain Res. 377:1986;173-176.
9. Chang D., Baram T. Z. Status epilepticus results in reversible neuronal injury in infant rat hippocampus: Novel use of a marker. Dev. Brain Res. 77:1994;133-136.
10. Chevalier G., Vacher S., Deniau J., Desban M. Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res. 334:1985;215-226.
11. Clifford D. B., Olney J. W., Maniotis A., Collins R. C., Zorumski C. F. The functional anatomy and pathology of lithium-pilocarpine and high doses pilocarpine seizures. Neuroscience. 23:1987;953-968.
12. Cooper I. S., Riklan M., Amin I., Cullinan T. A long-term follow-up study of cerebellar stimulation for the control of epilepsy. Cooper I. S. Cerebellar Stimulation in Man. 1978;19-38 Raven Press, New York.
13. Depaulis A., Vergnes M., Marescaux C. Endogenous control of epilepsy: The nigral inhibitory system. Prog. Neurobiol. 42:1994;33-55.
14. Deransart C., Vercueil L., Marescaux C., Depaulis A. The role of basal ganglia in the control of generalized absence seizures. Epilepsy Res. 32:1998;213-223.
15. Féger J., Robledo P. The effects of activation or inhibition of the subthalamic nucleus on the metabolic and electrophysiological activities within the pallidal complex and the substantia nigra in the rat. Eur. J. Neurosci. 3:1992;947-952.
16. Fernandes M. J. S., Boyet S., Marescaux C., Nehlig A. Correlation between hypermetabolism and neuronal damage during status epilepticus induced by lithium-pilocarpine in immature and adult rats. J. Cereb. Blood Flow Metab. 19:1999;195-209.
17. Folbergrova J., Ingvar M., Siesjö B. K. Metabolic changes in cerebral cortex, hippocampus and cerebellum during sustained bicuculline-induced seizures. J. Neurochem. 37:1981;1228-1238.
18. French J. A., Williamson P. D., Thadani V. M., Darcey T. M., Mattson R. H., Spencer S. S., Spencer D. D. Characteristics of medial temporal lobe epilepsy. I. Results of history and physical examination. Ann. Neurol. 34:1993;774-780.
19. Gallyas F., Hsu M., Buszaki G. Four modified silver methods for thick sections of formaldehyde-fixed mammalian central nervous tissue: 'Dark' neurons, perikarya of all neurons, microglial cells and capillaries. J. Neurosci. Methods. 50:1993;159-164.
20. Garant D. S., Gale K. Substantia nigra-mediated anticonvulsant actions: Role of nigral output pathways. Exp. Neurol. 97:1987;143-159.
21. Gerfen C. R., Staines W. A., Arbuthnott G. W., Fibiger H. C. Crossed connections of the substantia nigra in the rat. J. Comp. Neurol. 207:1982;283-303.
22. 14C-deoxyglucose study in the lithium-pilocarpine model in rat. Neuroscience. 64:1995;1057-1073.
23. 14C-deoxyglucose study. Neuroscience. 64:1995;1075-1089.
24. Holmes G. L. The long-term effects of seizures on the developing brain: Clinical and laboratory issues. Brain Dev. 13:1991;393-409.
25. Ingvar M. Cerebral blood flow and metabolic rate during seizures. Relationship to epileptic brain damage. Ann. N. Y. Acad. Sci. 462:1986;194-206.
26. Ingvar M., Folbergrova J., Siesjö B. K. Metabolic alterations underlying the development of hypermetabolic necrosis in the substantia nigra in status epilepticus. J. Cereb. Blood Flow Metab. 7:1987;103-108.
27. Löscher W., Czuczwar S. J., Jäkel R., Schwarz M. Effects of microinjections of γ-vinyl GABA or isoniazid into substantia nigra on the development of amygdala kindling in rats. Exp. Neurol. 95:1987;622-638.
28. 18F-2-deoxyglucose signal in PET activation studies. Mol. Psychiatry. 1:1996;445-452.
29. Mata M., Fink D. J., Gainer H., Smith C. B., Davidsen L., Savaki H., Schwartz W. K., Sokoloff L. Activity dependent energy metabolism in rat posterior pituitary primarily reflects sodium pump activity. J. Neurochem. 34:1980;213-215.
30. Mathern G. W., Kuhlman P. A., Mendoza D., Pretorius J. K. Human fascia dentata stratum granulosum and hilar areas, and hippocampal neuron counts differ depending on the epileptic syndrome and age at first seizures. J. Neuropathol. Exp. Neurol. 56:1997;199-212.
31. Mello L. E. A. M., Cavalheiro E. A., Tan A. M., Kupfer W. R., Pretorius J. K., Babb T. L., Finch D. M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: Cell loss and mossy fiber sprouting. Epilepsia. 34:1993;985-995.
32. Mello L. E. A. M., Covolan L. Spontaneous seizures preferentially injure interneurons in the pilocarpine model of chronic spontaneous seizures. Epilepsy Res. 26:1996;123-129.
33. Miller J. W., Gray B. C., Turner G. M. Role of the fastigial nucleus in generalized seizures as demonstrated by GABA agonist microinjections. Epilepsia. 34:1993;973-978.
34. Motte J., Fernandes M. J. S., Baram T. Z., Nehlig A. Spatial and temporal evolution of neuronal activation, stress and injury in lithium-pilocarpine seizures in adult rats. Brain Res. 793:1998;61-72.
35. Nehlig A., Pereira de Vasconcelos A. The model of pentylenetetrazol-induced status epilepticus in the immature rat: Short- and long-term effects. Epilepsy Res. 26:1996;93-103.
36. Nehlig A., Pereira de Vasconcelos A., Boyet S. Quantitative autoradiographic measurement of local cerebral glucose utilization in freely moving rats during postnatal development. J. Neurosci. 8:1988;2321-2333.
37. Nehlig A., Vergnes M., Boyet S., Marescaux C. Metabolic activity is increased in discrete brain regions before the occurrence of spike-and-wave discharges in weanling rats with genetic absence epilepsy. Dev. Brain Res. 108:1998;69-75.
38. Paz C., Gutiérrez-Baeza F., Bazán-Perkins B. Transection of the superior cerebellar peduncle interferes with the onset and duration of generalized seizures induced by amygdaloid kindling. Brain Res. 558:1991;90-92.
39. Pereira de Vasconcelos A., Boyet S., Nehlig A. Consequences of an early chronic phenobarbital treatment on postnatal evolution of local cerebral glucose utilization in the rat. Dev. Brain Res. 53:1990;168-178.
40. Pineau N., Charriaut-Marlangue C., Motte J., Nehlig A. Pentylenetetrazol induces cell suffering but not death in the immature rat brain. Dev. Brain Res. 112:1999;139-144.
41. Priel M. R., Ferreira dos Santos N., Cavalheiro E. A. Developmental aspects of the pilocarpine model of epilepsy. Epilepsy Res. 26:1996;115-121.
42. Shebab S., Dean P., Redgrave P. The dorsal midbrain anticonvulsant zone. II. Efferent connections revealed by the anterograde transport of wheatgerm agglutinin-horseradish peroxidase from injections centered on the intercollicular area in the rat. Neuroscience. 65:1995;681-695.
43. 14C]deoxyglucose method for the measurement of local cerebral glucose utilization: Theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28:1977;897-916.
44. Sperber E. F., Haas K. Z., Stanton P. K., Moshé S. L. Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Dev. Brain Res. 60:1991;88-93.
45. Takahashi S., Driscoll B. F., Law M. J., Sokoloff L. Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia. Proc. Natl. Acad. Sci. USA. 92:1995;4616-4620.
46. Tsacopoulos M., Magistretti P. J. Metabolic coupling between neurons and glia. J. Neurosci. 16:1996;877-885.
47. Turski L., Ikonomidou C., Turski W. A., Bortolotto Z. A., Cavalheiro E. A. Cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: A novel experimental model of intractable epilepsy. Synapse. 3:1989;154-171.
48. Waszczak B. L., Lee E. K., Walters R. J. Effects of anticonvulsant drugs on substantia nigra pars reticulata neurons. J. Pharmacol. Exp. Ther. 239:1986;606-611.