A single pentylenetetrazole-induced clonic-tonic seizure episode is accompanied by a slowly developing cognitive decline in rats

Epilepsy and Behavior

Volumn 26, Issue 2, 2013, Pages 196-202

  Aniol, Victor A ^a   Ivanova Dyatlova, Aleksandra Y ^a   Keren, Ora ^b   Guekht, Alla B ^c   Sarne, Yosef ^b   Gulyaeva, Natalia V ^a  

^a INSTITUTE OF HIGHER NERVOUS ACTIVITY AND NEUROPHYSIOLOGY   (Russian Federation)

^b TEL AVIV UNIVERSITY   (Israel)

^c PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

Author keywords

Cognitive impairments; Neurogenesis; Novel object recognition; Pentylenetetrazole; Radial arm maze; Seizure; Social recognition

Indexed keywords

PENTETRAZOLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; COGNITIVE DEFECT; CONTROLLED STUDY; HIPPOCAMPUS; MALE; NONHUMAN; RAT; RECOGNITION; SHORT TERM MEMORY; TONIC CLONIC SEIZURE;

ANIMALS; CELL PROLIFERATION; COGNITION DISORDERS; DISEASE PROGRESSION; HIPPOCAMPUS; MALE; MAZE LEARNING; PENTYLENETETRAZOLE; RATS; RATS, WISTAR; RECOGNITION (PSYCHOLOGY); SEIZURES;

EID: 84872601253     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2012.12.006     Document Type: Article

References (65)

1. Abrous D.N., Koehl M., Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 2005, 85(2):523-569.
2. Assaf F., Fishbein M., Gafni M., Keren O., Sarne Y. Pre- and post-conditioning treatment with an ultra-low dose of δ9-tetrahydrocannabinol (THC) protects against pentylenetetrazole (PTZ)-induced cognitive damage. Behav Brain Res 2011, 220(1):194-201.
3. Becker A., Braun H., Schröder H., Grecksch G., Höllt V. Effects of enadoline on the development of pentylenetetrazol kindling, learning performance, and hippocampal morphology. Brain Res 1999, 823(1-2):191-197.
4. Becker A., Tiedge A., Grecksch G.A. Diazepam-its effects on the development of pentylenetetrazol kindling, related learning impairments, and neuronal cell loss. Pharmacol Res 1997, 35(1):27-32.
5. Brooks-Kayal A. Molecular mechanisms of cognitive and behavioral comorbidities of epilepsy in children. Epilepsia 2011, 52(Suppl. 1):13-20.
6. Carreño M., Donaire A., Sánchez-Carpintero R. Cognitive disorders associated with epilepsy: diagnosis and treatment. Neurologist 2008, 14(6 Suppl. 1):S26-S34.
7. Cilio M.R., Sogawa Y., Cha B.H., Liu X., Huang L.T., Holmes G.L. Long-term effects of status epilepticus in the immature brain are specific for age and model. Epilepsia 2003, 44(4):518-528.
8. Cognato G.P., Agostinho P.M., Hockemeyer J., Müller C.E., Souza D.O., Cunha R.A. Caffeine and an adenosine A(2A) receptor antagonist prevent memory impairment and synaptotoxicity in adult rats triggered by a convulsive episode in early life. J Neurochem 2010, 112(2):453-462.
9. Cross D.J., Cavazos J.E. Synaptic reorganization in subiculum and CA3 after early-life status epilepticus in the kainic acid rat model. Epilepsy Res 2007, 73(2):156-165.
10. Dubé C., da Silva Fernandes M.J., Nehlig A. Age-dependent consequences of seizures and the development of temporal lobe epilepsy in the rat. Dev Neurosci 2001, 23(3):219-223.
11. Encinas J.M., Vaahtokari A., Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A 2006, 103(21):8233-8238.
12. Erdoǧan F., Gölgeli A., Arman F., Ersoy A.O. The effects of pentylenetetrazole-induced status epilepticus on behavior, emotional memory, and learning in rats. Epilepsy Behav 2004, 5(3):388-393.
13. Franke H., Kittner H. Morphological alterations of neurons and astrocytes and changes in emotional behavior in pentylenetetrazol-kindled rats. Pharmacol Biochem Behav 2001, 70(2-3):291-303.
14. Gascoigne M.B., Barton B., Webster R., Gill D., Antony J., Lah S.S. Accelerated long-term forgetting in children with idiopathic generalized epilepsy. Epilepsia 2012, [Epub ahead of print]. 10.1111/j.1528-1167.2012.03719.x.
15. Goldman H., Berman R.F., Hazlett J., Murphy S. Cerebrovascular responses to pentylenetetrazol: time and dose dependent effects. Epilepsy Res 1992, 12(3):227-242.
16. Genkova-Papazova M.G., Lazarova-Bakarova M.B. Pentylenetetrazole kindling impairs long-term memory in rats. Eur Neuropsychopharmacol 1995, 5(1):53-56.
17. Grecksch G., Becker A., Schroeder H., Höllt V. Involvement of delta-opioid receptors in pentylenetetrazol kindling development and kindling-related processes in rats. Naunyn Schmiedebergs Arch Pharmacol 1999, 360(2):151-156.
18. Gröticke I., Hoffmann K., Löscher W. Behavioral alterations in a mouse model of temporal lobe epilepsy induced by intrahippocampal injection of kainate. Exp Neurol 2008, 213(1):71-83.
19. Haas K.Z., Sperber E.F., Opanashuk L.A., Stanton P.K., Moshé S.L. Resistance of immature hippocampus to morphologic and physiologic alterations following status epilepticus or kindling. Hippocampus 2001, 11(6):615-625.
20. Hassan H., Grecksch G., Rüthrich H., Krug M. Effects of nicardipine, an antagonist of L-type voltage-dependent calcium channels, on kindling development, kindling-induced learning deficits and hippocampal potentiation phenomena. Neuropharmacology 1999, 38(12):1841-1850.
21. Hattiangady B., Kuruba R., Shetty A.K. Acute seizures in old age leads to a greater loss of CA1 pyramidal neurons, an increased propensity for developing chronic TLE and a severe cognitive dysfunction. Aging Dis 2011, 2(1):1-17.
22. Holmes G.L., Gairsa J.L., Chevassus-Au-Louis N., Ben-Ari Y. Consequences of neonatal seizures in the rat: morphological and behavioral effects. Ann Neurol 1998, 44(6):845-857.
23. Holmes G.L., Sarkisian M., Ben-Ari Y., Chevassus-Au-Louis N. Mossy fiber sprouting after recurrent seizures during early development in rats. J Comp Neurol 1999, 404(4):537-553.
24. Hort J., Brozek G., Komárek V., Langmeier M., Mares P. Interstrain differences in cognitive functions in rats in relation to status epilepticus. Behav Brain Res 2000, 112(1-2):77-83.
25. Jessberger S., Clark R.E., Broadbent N.J., et al. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 2009, 16(2):147-154.
26. Jessberger S., Nakashima K., Clemenson G.D., et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 2007, 27(22):5967-5975.
27. Jiang W., Wan Q., Zhang Z.J., et al. Dentate granule cell neurogenesis after seizures induced by pentylenetrazol in rats. Brain Res 2003, 977(2):141-148.
28. Kadar T., Cohen G., Sahar R., Alkalai D., Shapira S. Long-term study of brain lesions following soman, in comparison to DFP and metrazol poisoning. Hum Exp Toxicol 1992, 11(6):517-523.
29. Kasof G.M., Mandelzys A., Maika S.D., Hammer R.E., Curran T., Morgan J.I. Kainic acid-induced neuronal death is associated with DNA damage and a unique immediate-early gene response in c-fos-lacZ transgenic rats. J Neurosci 1995, 15(6):4238-4249.
30. Kempermann G. Youth culture in the adult brain. Science 2012, 335(6073):1175-1176.
31. Kim D.H., Yoon B.H., Jung W.Y., et al. Sinapic acid attenuates kainic acid-induced hippocampal neuronal damage in mice. Neuropharmacology 2010, 59(1-2):20-30.
32. Kokaia M. Seizure-induced neurogenesis in the adult brain. Eur J Neurosci 2011, 33(6):1133-1138.
33. Kunz T., Marklund N., Hillered L., Oliw E.H. Assessment of the effects of the cyclooxygenase-2 inhibitor rofecoxib on visuospatial learning and hippocampal cell death following kainate-induced seizures in the rat. Brain Res Cogn Brain Res 2005, 25(3):826-832.
34. Letty S., Lerner-Natoli M., Rondouin G. Differential impairments of spatial memory and social behavior in two models of limbic epilepsy. Epilepsia 1995, 36(10):973-982.
35. Liu Z., Gatt A., Werner S.J., Mikati M.A., Holmes G.L. Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res 1994, 19(3):191-204.
36. Majak K., Pitkänen A. Do seizures cause irreversible cognitive damage? Evidence from animal studies. Epilepsy Behav 2004, 5(Suppl. 1):S35-S44.
37. Mikati M.A., Tarif S., Lteif L., Jawad M.A. Time sequence and types of memory deficits after experimental status epilepticus. Epilepsy Res 2001, 43(2):97-101.
38. Miltiadous P., Stamatakis A., Koutsoudaki P.N., Tiniakos D.G., Stylianopoulou F. IGF-I ameliorates hippocampal neurodegeneration and protects against cognitive deficits in an animal model of temporal lobe epilepsy. Exp Neurol 2011, 231(2):223-235.
39. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005, 28:223-250.
40. Mohajeri M.H., Saini K., Li H., et al. Intact spatial memory in mice with seizure-induced partial loss of hippocampal pyramidal neurons. Neurobiol Dis 2003, 12(3):174-181.
41. Mortazavi F., Ericson M., Story D., Hulce V.D., Dunbar G.L. Spatial learning deficits and emotional impairments in pentylenetetrazole-kindled rats. Epilepsy Behav 2005, 7(4):629-638.
42. Nakagawa E., Aimi Y., Yasuhara O., et al. Enhancement of progenitor cell division in the dentate gyrus triggered by initial limbic seizures in rat models of epilepsy. Epilepsia 2000, 41(1):10-18.
43. Obeid M., Frank J., Medina M., et al. Neuroprotective effects of leptin following kainic acid-induced status epilepticus. Epilepsy Behav 2010, 19(3):278-283.
44. Omrani A., Ghadami M.R., Fathi N., Tahmasian M., Fathollahi Y., Touhidi A. Naloxone improves impairment of spatial performance induced by pentylenetetrazol kindling in rats. Neuroscience 2007, 145(3):824-831.
45. Panegyres P.K. The effects of excitotoxicity on the expression of the amyloid precursor protein gene in the brain and its modulation by neuroprotective agents. J Neural Transm 1998, 105(4-5):463-478.
46. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997, 17(10):3727-3738.
47. Pavlova T.V., Stepanichev M.Y., Gekht A.B., Gulyaeva N.V. Acquisition of an active avoidance reaction in rats and morphological changes in the hippocampus in pentylenetetrazol kindling. Neurosci Behav Physiol 2010, 40(5):501-506.
48. Pavlova T.V., Yakovlev A.A., Stepanichev M.Y., Gulyaeva N.V. Pentylenetetrazol kindling in rats: is neurodegeneration associated with manifestations of convulsive activity?. Neurosci Behav Physiol 2006, 36(7):741-748.
49. Pereno G., Beltramino C. Understanding the pathophysiology of epilepsy in an animal model: pentylenetetrazole induces activation but not death of neurons of the medial extended amygdala. Neurologia 2010, 25(3):148-155.
50. Persinger M.A., Bureau Y.R., Kostakos M., Peredery O., Falter H. Behaviors of rats with insidious, multifocal brain damage induced by seizures following single peripheral injections of lithium and pilocarpine. Physiol Behav 1993, 53(5):849-866.
51. Persinger M.A., Bureau Y.R., Peredery O. Dissociation between conditioned taste aversion and radial maze learning following seizure-induced multifocal brain damage: quantitative tests of serial vs. parallel circuit models of memory. Physiol Behav 1994, 56(2):225-235.
52. Planas A.M., Soriano M.A., Ferrer I., Rodriguez Farré E. Regional expression of inducible heat shock protein-70 mRNA in the rat brain following administration of convulsant drugs. Brain Res Mol Brain Res 1994, 27(1):127-137.
53. Pohle W., Becker A., Grecksch G., Juhre A., Willenberg A. Piracetam prevents pentylenetetrazol kindling-induced neuronal loss and learning deficits. Seizure 1997, 6(6):467-474.
54. Rösche J., Uhlmann C., Fröscher W. Cognitive deficits and psychiatric disorders in patients with new-onset epilepsy. Fortschr Neurol Psychiatr 2010, 78(1):18-26.
55. Rüthrich H., Grecksch G., Krug M. Development of long-lasting potentiation effects in the dentate gyrus during pentylenetetrazol kindling. Int J Dev Neurosci 2001, 19(3):247-254.
56. Scharfman H.E. Epilepsy as an example of neural plasticity. Neuroscientist 2002, 8(2):154-173.
57. Scharfman H.E. Functional implications of seizure-induced neurogenesis. Adv Exp Med Biol 2004, 548:192-212.
58. Scorza F.A., Arida R.M., Naffah-Mazzacoratti Mda G., Scerni D.A., Calderazzo L., Cavalheiro E.A. The pilocarpine model of epilepsy: what have we learned?. An Acad Bras Cienc 2009, 81(3):345-365.
59. Sroubek J., Hort J., Komárek V., Langmeier M., Brozek G. Acquisition and retrieval of conditioned taste aversion is impaired by brain damage caused by two hours of pilocarpine-induced status epilepticus. Physiol Res 2001, 50(6):609-617.
60. Szyndler J., Piechal A., Blecharz-Klin K., et al. Effect of kindled seizures on rat behavior in water Morris maze test and amino acid concentrations in brain structures. Pharmacol Rep 2006, 58(1):75-82.
61. Von Bohlen und Halbach O. Immunohistological markers for staging neurogenesis in adult hippocampus. Cell Tissue Res 2007, 329(3):409-420.
62. Wood J.C., Jackson J.S., Jakubs K., et al. Functional integration of new hippocampal neurons following insults to the adult brain is determined by characteristics of pathological environment. Exp Neurol 2011, 229(2):484-493.
63. Yang Y., Liu Z., Cermak J.M., et al. Protective effects of prenatal choline supplementation on seizure-induced memory impairment. J Neurosci 2000, 20(22):RC109.
64. Yasuda M., Johnson-Venkatesh E.M., Zhang H., Parent J.M., Sutton M.A., Umemori H. Multiple forms of activity-dependent competition refine hippocampal circuits in vivo. Neuron 2011, 70(6):1128-1142.
65. Yin S., Guan Z., Tang Y., Zhao J., Hong J., Zhang W. Abnormal expression of epilepsy-related gene ERG1/NSF in the spontaneous recurrent seizure rats with spatial learning memory deficits induced by kainic acid. Brain Res 2005, 1053(1-2):195-202.