Development of later life spontaneous seizures in a rodent model of hypoxia-induced neonatal seizures

Epilepsia

Volumn 52, Issue 4, 2011, Pages 753-765

  Rakhade, Sanjay N ^a   Klein, Peter M ^a   Huynh, Thanthao ^a   Hilario Gomez, Cristina ^a   Kosaras, Bela ^a   Rotenberg, Alexander ^a   Jensen, Frances E ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Animal model; Electroencephalography; Epilepsy; Infant; Neonatal seizures

Indexed keywords

PHENOBARBITAL;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE DURATION; EARLY LIFE STRESS; ELECTROENCEPHALOGRAPHY; HIPPOCAMPAL MOSSY FIBER; HYPOXIA; IMMUNOHISTOCHEMISTRY; LONG EVANS RAT; MALE; NERVE CELL NECROSIS; NERVE SPROUTING; NEWBORN DISEASE; NONHUMAN; ONSET AGE; PERINATAL PERIOD; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SEIZURE; SINGLE DRUG DOSE;

ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; EPILEPSY; HUMANS; HYPOXIA, BRAIN; INFANT, NEWBORN; RATS; RATS, LONG-EVANS; SEIZURES;

EID: 79953677204     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2011.02992.x     Document Type: Article

References (71)

1. Amaral DG,. (1979) Synaptic extensions from the mossy fibers of the fascia dentata. Anat Embryol (Berl) 155: 241-251. (Pubitemid 9202357)
2. Babb TL,. (1991) Bilateral pathological damage in temporal lobe epilepsy. Can J Neurol Sci 18: 645-648.
3. Baram TZ, Eghbal-Ahmadi M, Bender RA,. (2002) Is neuronal death required for seizure-induced epileptogenesis in the immature brain? Prog Brain Res 135: 365-375. (Pubitemid 35461032)
4. Ben Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R,. (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6: 1361-1391. (Pubitemid 11074864)
5. Berg AT, Shinnar S,. (1997) Do seizures beget seizures? An assessment of the clinical evidence in humans. Clin Neurophysiol 14: 102-110. (Pubitemid 28246500)
6. Berg AT, Levy SR, Novotny EJ, Shinnar S,. (1996) Predictors of intractable epilepsy in childhood: a case-control study. Epilepsia 37: 24-30. (Pubitemid 26021572)
7. Camfield P, Camfield C,. (2002) Epileptic syndromes in childhood: clinical features, outcomes, and treatment. Epilepsia 43 (suppl 3): 27-32. (Pubitemid 34633695)
8. Cha BH, Akman C, Silveira DC, Liu X, Holmes GL,. (2004) Spontaneous recurrent seizure following status epilepticus enhances dentate gyrus neurogenesis. Brain Dev 26: 394-397. (Pubitemid 38953328)
9. Cherubini E, DeFeo MR, Mecarelli O, Ricci GF,. (1983) Behavioral and electrographic patterns induced by systemic administration of kainic acid in developing rats. Dev Brain Res 9: 69-77. (Pubitemid 13034302)
10. Cronin J, Dudek FE,. (1988) Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 474: 181-184. (Pubitemid 19001195)
11. Crusio WE, Schwegler H, Lipp HP,. (1987) Radial-maze performance and structural variation of the hippocampus in mice: a correlation with mossy fibre distribution. Brain Res 425: 182-185. (Pubitemid 17159383)
12. D'Ambrosio R, Fairbanks JP, Fender JS, Born DE, Doyle DL, Miller JW,. (2004) Post-traumatic epilepsy following fluid percussion injury in the rat. Brain 127: 304-314. (Pubitemid 38160315)
13. D'Ambrosio R, Hakimian S, Stewart T, Verley DR, Fender JS, Eastman CL, Sheerin AH, Gupta P, Diaz-Arrastia R, Ojemann J, Miller JW,. (2009) Functional definition of seizure provides new insight into post-traumatic epileptogenesis. Brain 132: 2805-2821.
14. Dube C, Baram TZ, Pitkanen A, Schwartzkroin PA,. (2005) Complex febrile seizures-an experimental model in immature rodent. Models of seizures and epilepsy. Elsevier, San Diego, pp. 333-340.
15. Dube C, Richichi C, Bender RA, Chung G, Litt B, Baram TZ,. (2006) Temporal lobe epilepsy after experimental prolonged febrile seizures: prospective analysis. Brain 129: 911-922.
16. Dudek FE, Hellier JL, Williams PA, Ferraro DJ, Staley KJ,. (2002) The course of cellular alterations associated with the development of spontaneous seizures after status epilepticus. Prog Brain Res 135: 53-65. (Pubitemid 35461006)
17. Dudek FE, Ekstrand JJ, Staley KJ,. (2010) Is neuronal death necessary for acquired epileptogenesis in the immature brain? Epilepsy Curr 10: 95-99.
18. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ,. (2005) NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11: 1205-1213. (Pubitemid 43093668)
19. Dzhala VI, Brumback AC, Staley KJ,. (2008) Bumetanide enhances phenobarbital efficacy in a neonatal seizure model. Ann Neurol 63: 222-235. (Pubitemid 351355301)
20. Glass HC, Glidden D, Jeremy RJ, Barkovich AJ, Ferriero DM, Miller SP,. (2009) Clinical neonatal seizures are independently associated with outcome in infants at risk for hypoxic-ischemic brain injury. J Pediatr 155: 318-323.
21. Golarai G, Cavazos JE, Sutula TP,. (1992) Activation of the dentate gyrus by pentylenetetrazol evoked seizures induces mossy fiber synaptic reorganization. Brain Res 593: 257-264.
22. Hauser WA, Annegers JF, Kurland LT,. (1993) Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935-1984. Epilepsia 34: 453-468. (Pubitemid 23184580)
23. Hermann BP, Seidenberg M, Bell B,. (2002) The neurodevelopmental impact of childhood onset temporal lobe epilepsy on brain structure and function and the risk of progressive cognitive effects. Prog Brain Res 135: 429-438. (Pubitemid 35461039)
24. Holmes GL,. (2005) Effects of seizures on brain development: lessons from the laboratory. Pediatr Neurol 33: 1-11. (Pubitemid 40910207)
25. Holmes GL,. (2009) The long-term effects of neonatal seizures. Clin Perinatol 36: 901-914.
26. Holmes GL, Gaiarsa JL, Chevassus-Au-Louis N, Ben-Ari Y,. (1998) Consequences of neonatal seizures in the rat: morphological and behavioral effects. Ann Neurol 44: 845-857. (Pubitemid 28558245)
27. Holmes GL, Sarkisian M, Ben-Ari Y, Chevassus-Au-Louis N,. (1999) Mossy fiber sprouting after recurrent seizures during early development in rats. J Comp Neurol 404: 537-553. (Pubitemid 29084640)
28. Huang L, Cilio MR, Silveira DC, McCabe BK, Sogawa Y, Stafstrom CE, Holmes GL,. (1999) Long-term effects of neonatal seizures: a behavioral, electrophysiological, and histological study. Brain Res Dev Brain Res 118: 99-107. (Pubitemid 30009642)
29. Ives JR,. (2005) New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol 22: 119-123. (Pubitemid 40490403)
30. Jensen FE,. (1999) Acute and chronic effects of seizures in the developing brain: experimental models. Epilepsia 40 (suppl 1): S51-S58. (Pubitemid 29367114)
31. Jensen FE, Applegate CD, Holtzman D, Belin T, Burchfiel J,. (1991) Epileptogenic effect of hypoxia in the immature rodent brain. Ann Neurol 29: 629-637.
32. Jensen FE, Holmes GL, Lombroso CT, Blume HK, Firkusny IR,. (1992) Age dependent changes in long term seizure susceptibility and behavior after hypoxia in rats. Epilepsia 33: 971-980. (Pubitemid 23005252)
33. Jensen FE, Alvarado S, Firkusny IR, Geary C,. (1995) NBQX blocks the acute and late epileptogenic effects of perinatal hypoxia. Epilepsia 36: 966-972.
34. Jensen FE, Wang C, Stafstrom CE, Liu Z, Geary C, Stevens MC,. (1998) Acute and chronic increases in excitability in rat hippocampal slices after perinatal hypoxia in vivo. J Neurophysiol 79: 73-81. (Pubitemid 28133800)
35. Kadam SD, White AM, Staley KJ, Dudek FE,. (2010) Continuous electroencephalographic monitoring with radio-telemetry in a rat model of perinatal hypoxia-ischemia reveals progressive post-stroke epilepsy. J Neurosci 30: 404-415.
36. Karnam HB, Zhou JL, Huang LT, Zhao Q, Shatskikh T, Holmes GL,. (2009) Early life seizures cause long-standing impairment of the hippocampal map. Exp Neurol 217: 378-387.
37. Koh S, Jensen FE,. (2001) Topiramate blocks perinatal hypoxia-induced seizures in rat pups. Ann Neurol 50: 366-372. (Pubitemid 32848739)
38. Koh S, Tibayan FD, Simpson J, Jensen FE,. (2004) NBQX or topiramate treatment following perinatal hypoxia-induced seizures prevents later increases in seizure-induced neuronal injury. Epilepsia 45: 569-575. (Pubitemid 38802202)
39. Liu Z, Gatt A, Werner SJ, Mikati MA, Holmes GL,. (1994) Long term behavioral defects following pilocarpine seizures in immature rats. Epilepsy Res 19: 191-204.
40. Meikle L, Talos DM, Onda H, Pollizzi K, Rotenberg A, Sahin M, Jensen FE, Kwiatkowski DJ,. (2007) A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival. J Neurosci 27: 5546-5558. (Pubitemid 350021088)
41. Mikati MA, Zeinieh MP, Kurdi RM, Harb SA, El Hokayem JA, Daderian RH, Shamseddine A, Obeid M, Bitar FF, El Sabban M,. (2005) Long-term effects of acute and of chronic hypoxia on behavior and on hippocampal histology in the developing brain. Brain Res Dev Brain Res 157: 98-102. (Pubitemid 40812949)
42. Mizrahi EM,. (1987) Neonatal seizures: problems in diagnosis and classification. Epilepsia 28 (suppl 1): S46-S55.
43. Rahimi O, Claiborne BJ,. (2007) Morphological development and maturation of granule neuron dendrites in the rat dentate gyrus. Prog Brain Res 163: 167-181. (Pubitemid 47321435)
44. Rakhade SN, Jensen FE,. (2009) Epileptogenesis in the immature brain: emerging mechanisms. Nat Rev Neurol 5: 380-391.
45. Rakhade SN, Zhou C, Aujla PK, Fishman R, Sucher NJ, Jensen FE,. (2008) Early alterations of AMPA receptors mediate synaptic potentiation induced by neonatal seizures. J Neurosci 28: 7979-7990.
46. Raol YH, Lapides DA, Keating JG, Brooks-Kayal AR, Cooper EC,. (2009) A KCNQ channel opener for experimental neonatal seizures and status epilepticus. Ann Neurol 65: 326-336.
47. Represa A, Ben-Ari Y,. (1992) Kindling is associated with the formation of novel mossy fibre synapses in the CA3 region. Exp Brain Res 92: 69-78. (Pubitemid 23006357)
48. Ribak CE, Baram TZ,. (1996) Selective death of hippocampal CA3 pyramidal cells with mossy fiber afferents after CRH-induced status epilepticus in infant rats. Brain Res Dev Brain Res 91: 245-251. (Pubitemid 26069873)
49. Ronen GM, Buckley D, Penney S, Streiner DL,. (2007) Long-term prognosis in children with neonatal seizures: a population-based study. Neurology 69: 1816-1822. (Pubitemid 350071141)
50. Rotenberg A, Muller P, Birnbaum D, Harrington M, Riviello JJ, Pascual-Leone A, Jensen FE,. (2008) Seizure suppression by EEG-guided repetitive transcranial magnetic stimulation in the rat. Clin Neurophysiol 119: 2697-2702.
51. Sanchez RM, Koh S, Rio C, Wang C, Lamperti ED, Sharma D, Corfas G, Jensen FE,. (2001) Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J Neurosci 21: 8154-8163. (Pubitemid 32952771)
52. Sanchez RM, Dai W, Levada RE, Lippman JJ, Jensen FE,. (2005a) AMPA/kainate receptor-mediated downregulation of GABAergic synaptic transmission by calcineurin after seizures in the developing rat brain. J Neurosci 25: 3442-3451. (Pubitemid 40471352)
53. Sanchez RM, Jensen FE, Pitanken A, Schwartzkroin PA, Moshe SL,. (2005b) Modeling hypoxia-induced seizures and hypoxic encephalopathy in the neonatal period. Models of seizures and epilepsy. Elsevier Press, San Diego.
54. Sankar R, Painter MJ,. (2005) Neonatal seizures: after all these years we still love what doesn't work. Neurology 64: 776-777. (Pubitemid 40316310)
55. Schmid R, Tandon P, Stafstrom CE, Holmes GL,. (1999) Effects of neonatal seizures on subsequent seizure-induced brain injury. Neurology 53: 1754-1761. (Pubitemid 29530351)
56. Schmued LC, Stowers CC, Scallet AC, Xu L,. (2005) Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res 1035: 24-31. (Pubitemid 40248533)
57. Schwegler H, Crusio WE, Lipp HP, Heimrich B,. (1988) Water-maze learning in the mouse correlates with variation in hippocampal morphology. Behav Genet 18: 153-165.
58. Shaw FZ,. (2007) 7-12 Hz high-voltage rhythmic spike discharges in rats evaluated by antiepileptic drugs and flicker stimulation. J Neurophysiol 97: 238-247.
59. Silverstein FS, Jensen FE,. (2007) Neonatal seizures. Ann Neurol 62: 112-120. (Pubitemid 47546496)
60. Smith KL, Lee CL, Swann JW,. (1998) Local cicuit abnormalities in chronically epileptic rats after intrahippocampal tetanus toxin injection in infancy. J Neurophysiol 79: 106-116. (Pubitemid 28133803)
61. Sogawa Y, Monokoshi M, Silveira DC, Cha BH, Cilio MR, McCabe BK, Liu X, Hu Y, Holmes GL,. (2001) Timing of cognitive deficits following neonatal seizures: relationship to histological changes in the hippocampus. Brain Res Dev Brain Res 131: 73-83. (Pubitemid 33079220)
62. Soria C, El Sabbagh S, Escolano S, Bobet R, Bulteau C, Dellatolas G,. (2007) Quality of life in children with epilepsy and cognitive impairment: a review and a pilot study. Dev Neurorehabil 10: 213-221. (Pubitemid 47555453)
63. Stafstrom CE, Tandon P, Hori A, Liu Z, Mikati MA, Holmes GL,. (1997) Acute effects of MK801 on kainic acid-induced seizures in neonatal rats. Epilepsy Res 26: 335-344. (Pubitemid 27117809)
64. Sutula T, He XX, Cavazos J, Scott G,. (1988) Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239: 1147-1150. (Pubitemid 18084325)
65. Sutula T, Cascino G, Cavazos J, Parada I, Ramirez L,. (1989) Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 26: 321-330. (Pubitemid 19230299)
66. Talos DM, Fishman RE, Park H, Folkerth RD, Follett PL, Volpe JJ, Jensen FE,. (2006) Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4- isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. J Comp Neurol 497: 42-60. (Pubitemid 43844567)
67. Tauck DL, Nadler JV,. (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5: 1016-1022. (Pubitemid 15123049)
68. Tekgul H, Gauvreau K, Soul J, Stewart J, Volpe JJ, Bourgeois B, du Plessis A,. (2006) The current etiologic profile and neurodevelopmental outcome of seizures in term newborn infants. Pediatrics 117: 1270-1280. (Pubitemid 46071521)
69. Toet MC, Groenendaal F, Osredkar D, van Huffelen AC, de Vries LS,. (2005) Postneonatal epilepsy following amplitude-integrated EEG-detected neonatal seizures. Pediatr Neurol 32: 241-247. (Pubitemid 40410646)
70. Volpe JJ,. (2008) Neurology of the newborn. Saunders/Elsevier, Philadelphia.
71. Wuarin JP, Dudek FE,. (1996) Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 16: 4438-4448. (Pubitemid 26243039)