Mossy fiber sprouting after recurrent seizures during early development in rats

Journal of Comparative Neurology

Volumn 404, Issue 4, 1999, Pages 537-553

  Holmes, Gregory L ^a,b   Sarkisian, Matthew ^a   Ben Ari, Yehezkel ^b   Chevassus Au Louis, Nicolas ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b INSERM   (France)

Author keywords

Epilepsy; Pentylenetetrazol; Synapses

Indexed keywords

PENTETRAZOLE;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN DEVELOPMENT; BRAIN SLICE; CELL COUNT; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; HIPPOCAMPUS; MOSSY FIBER; NERVE FIBER REGENERATION; NEUROPATHOLOGY; NEWBORN; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; RAT; REFLEX EPILEPSY; SCORING SYSTEM; SEIZURE; SEIZURE THRESHOLD;

EID: 0033593821     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19990222)404:4<537::aid-cne9>3.0.co;2-%23     Document Type: Article

References (100)

1. Albala BJ, Moshé SL, Okada R. 1984. Kainic-acid-induced seizures: A developmental study. Dev Brain Res 13:139-148.
2. Amaral DG, Dent JA. 1981. Development of the mossy fibers of the dentate gyrus: I. Alight and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
3. Acsády L, Kamondi A, Sik A, Freund T, Buzsáki G. 1998. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neursosci 18:3386-3403.
4. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF. 1991. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42:351-363.
5. Baram TZ, Ribak CE. 1995. Peptide-induced infant status epilepticus causes neuronal death and synaptic reorganization. NeuroReport 6:277-280.
6. 3H-thymidine autoradiography. J Comp Neurol 190:87-114.
7. A, NMDA and AMPA receptors: A developmentally regulated "ménage à trois." TINS J 20:523-529.
8. Bengzon J, Kokaia Z, Elmér E, Nanobashvili A, Kokaia M, Lindvall O. 1997. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 94:10432-10437.
9. Bourgeois BFD, Prensky AL, Palkes HS, Talent BK, Busch SG. 1983. Intelligence in epilepsy: A prospective study in children. Ann Neurol 14:438-444.
10. Cavalheiro EA, Silva DF, Turski WA, Calderazzo-Filho LS, Bortolotto ZA, Turski L. 1987. The susceptibility of rats to pilocarpine-induced seizures is age-dependent. Dev Brain Res 37:43-58.
11. Cavazos JE, Sutula TP. 1990. Progressive neuronal loss induced by kindling: A possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis. Brain Res 527:1-6.
12. Cavazos JE, Golarai G, Sutula TP. 1991. Mossy fiber synaptic reorganization induced by kindling: Time course of development, progression, and permanence. J Neurosci 11:2795-2803.
13. Cheema SS, Lauder JM. 1983. Infrapyramidal mossy fibers in the hippocampus of methylazoxymethanol acetate-induced microcephalic rats. Dev Brain Res 9:411-415.
14. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: A case for more uniform standards of review. J Comp Neurol 364:6-15.
15. 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.
16. Crusio WE, Schwegler H, Lipp H-P. 1987. Radial-maze performance and structural variation of the hippocampus in mice: A correlation with mossy fibre distribution. Brain Res 425:182-185.
17. DeLorenzo RJ, Towne AR, Pellock JM, Ko D. 1992. Status epilepticus in children, adults, and the elderly. Epilepsia Suppl. 4 33:S15-S25.
18. Funakoshi A, Morikawa T, Muramatsu R, Yagi K, Seino M. 1988. A propsective WISC-R study in children with epilepsy. Jpn J Psychiatr Neurol 42:562-564.
19. Gaarskjaer FB. 1978a. Organization of the mossy fiber system of the rat studied in extended hippocampi. I. Terminal area related to number of granule and pyramidal cells. J Comp Neur 178:49-72.
20. Gaarskjaer FB. 1978b. Organization of the mossy fiber system of the rat studied in extended hippocampi. II. Experimental analysis of fiber distribution with silver impregnation methods. J Comp Neur 178: 73-88.
21. Gaarskjaer FB. 1986. The organization and development of the hippocampal mossy fiber system. Brain Res Rev 11:335-357.
22. 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.
23. Gomez MR, Kuntz NL, Westmoreland BF. 1982. Tuberous sclerosis, early onset of seizures, and mental subnormality: Study of discordant homozygous twins. Neurology 32:604-611.
24. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. 1998. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168-3171.
25. Guillery RW, Herrup K. 1997. Quantification without pontification: Choosing a method of counting objects in sectioned tissues. J Comp Neurol 386:2-7.
26. Hartmann D, Frotscher M, Sievers J. 1994. Development of granule cells, and afferent and efferent connections of the dentate gyrus after experimentally induced reorganization of the supra- and infrapyramidal blades. J Neurosci Res 35:419-427.
27. Hauser WA, Hersdorffer DC. 1990. Epilepsy: Frequency, Causes and Consequences. New York: Demos.
28. Hirsch E, Baram TZ, Snead III OC. 1992. Ontogenic study of lithium-pilocarpine-induced status epilepticus in rats. Brain Res 583:120-126.
29. Holmes GL. 1991a. Do seizures cause brain damage? Epilepsia Suppl. 5 32:S14-S28.
30. Holmes GL. 199 Ib. The long-term effects of seizures on the developing brain: Clinical and laboratory issues. Brain Dev 13:393-409.
31. Holmes GL. 1997a. Epilepsy in the developing brain: Lessons from the laboratory and clinic. Epilepsia 38:12-30.
32. Holmes GL. 1997b. Epilepsy and other seizure disorders. In: Berg B, editor. Principles of pediatric neurology. New York: McGraw-Hill, Inc. p 223-284.
33. Holmes GL, Moshé SL. 1990. Consequences of seizures in the developing brain. J Epilepsy Suppl 3:7-13.
34. Holmes GL, Thompson JL. 1987. Rapid kindling in the prepubescent rat. Brain Res 433:281-284.
35. Holmes GL, Weber DA. 1983. Increased susceptibility to pentylenetetrazol-induced seizures in adult rats following electrical kindling during brain development. Dev Brain Res 11:312-314.
36. Holmes GL, Thompson JL, Marchi T, Feldman DS 1988. Behavioral effects of kainic acid administration on the immature brain. Epilepsia 29:721-730.
37. Holmes GL, Gairsa J-L, Chevassus-Au-Louis N, Yang Y, Ben-Ari Y. 1998. Consequences of neonatal seizures in the rat: Morphological and behavioral effects. Ann Neurol, in press.
38. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV. 1990. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10:267-282.
39. Isokawa M, Levesque MF, Babb TL, Engel J, Jr. 1993. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy. J Neurosci 13:1511-1522.
40. Jensen FE, Applegate CD, Holzman D, Belin TR, Burchfiel JL. 1991. Epileptogenic effect of hypoxia in the immature rodent brain. Ann Neurol 29:629-637.
41. Kaplan MS, Hind JW. 1977. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 197:1092-1094.
42. Khazipov R, Leinekugel X, Khalilov I, Gaiarsa J-L, Ben-Ari Y. 1997. Synchronization of GABAergic interneuronal network in CA3 subfield of neonatal rat hippocampal slices. J Physiol 498:763-772.
43. Laurberg S, Zimmer J. 1980. Lesion-induced rerouting of hippocampal mossy fibers in developing but not in adult rats. J Comp Neurol 190:627-650.
44. Leite JP, Babb TL, Pretorius JK, Kuhlman PA, Yeoman KM, Mathern GW. 1996. Neuron loss, mossy fiber sprouting, and interictal spikes after intrahippocampal kainate in developing rats. Epilepsy Res 26:219-231.
45. Lipp H-P, Schwegler H, Driscoll P. 1984. Postnatal modification of hippocampal circuitry alters avoidance learning in adult rats. Science 225:80-82.
46. Lipp H-P, Schwegler H, Heimrich B, Driscoll P. 1988. Infrapyramidal mossy fibers and two-way avoidance learning: Developmental modification of hippocampal circuitry and adult behavior of rats and mice. J Neurosci 8:1905-1921.
47. Lin Z, Gatt A, Mikati M. Holmes GL. 1995. Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res 19:191-204.
48. Masukawa LM, O'Connor WM, Lynott J, Burdette LJ, Uruno K, McGonigle P, O'Connor MJ. 1995. Longitudinal variation in cell density and mossy fiber reorganization in the dentate gyrus from temporal lobe epileptic patients. Brain Res 678:65-75.
49. Mathern GW, Leite JP, Pretorius JK, Quinn B. Peacock WJ, Babb TL. 1994. Children with severe epilepsy: Evidence of hippocampal neuron losses and aberrant mossy fiber sprouting during postnatal granule cell migration and differentiation. Dev Brain Res 78:70-80.
50. Mathern GW, Babb TL, Mischel PS, Vinters HV, Pretorius JK, Leite JP, Peacock WJ. 1996. Childhood generalized and mesial temporal epilepsies demonstrate different amounts and patterns of hippocampal neuron loss and mossy fibre synaptic reorganization. Brain 119:965-987.
51. McNamara JO. 1994. Cellular and molecular basis of epilepsy. J Neurosci 14:3413-3425.
52. Meldrum BS, Brierley JB. 1973. Prolonged epileptic seizures in primates: Ischaemic cell change and its relation to ictal physiological events. Arch Neurol 28:10-17.
53. Meldrum BS, Vigoureux RA, Brierley JB. 1973. Systemic factors and epileptic brain damage. Prolonged seizures in paralysed artificially ventilated baboons. Arch Neurol 29:82-87.
54. Moshé SL. 1981. The effects of age on the kindling phenomenon. Dev Psychobiol 14:75-81.
55. Moshé SL, Albala BJ, Ackermann RF, Engel JJ. 1983. Increased seizure susceptibility of the immature brain. Dev Brain Res 7:81-85.
56. Moshé SL, Velisek L, Holmes GL. 1994. Developmental aspects of experimental generalized seizures induced by pentylenetetrazol, bicuculline and flurothyl. In: Malafosse A, Genton P, Hirsch E, Marescaux C, Broglin D, Bernasconi R, editors. Idiopathic Generalized Epilepsies. London: John Libbey. p 51-64.
57. Moshé SL, Shinnar S, Swann JW. 1995. Partial (focal) seizures in developing brain. In: Schwartzkroin PA, Moshé SL, Noebels SL, Swann JW, editors. Brain Development and Epilepsy. New York: Oxford University Press, p 34-65.
58. Nadler JV. 1981. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 29:2031-2042.
59. Nadler JV, Perry BW, Cotman CW. 1978. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 271:676-677.
60. Neill J, Liu Z, Sarkisian M, Tandon P, Yang Y, Stafstrom CE, Holmes GL. 1996. Recurrent seizures in immature rats: Effect on auditory and visual discrimination. Dev Brain Res 95:283-292.
61. Nitecka L, Tremblay E, Charton G, Bouillot JP, Berger M, Ben-Ari Y. 1984. Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae. Neuroscience 13:1073-1094.
62. Okazaki ME, Evenson DA, Nadler JV. 1995. Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: Visualization after retrograde transport of biocytin. J Comp Neurol 352:515-534.
63. Olney JW, Fuller T, De Gubareff T. 1979. Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res 176:91-100.
64. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. 1997. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network plasticity in the adult hippocampus. J Neurosci 17:3727-3738.
65. Paxinos G, Watson C. 1982. The Rat Brain in Stereotaxic Coordinates. Syndney: Academic Press.
66. Ramanjaneyulu R, Ticku MK. 1984. Interactions of pentamethylenetetrazol and tetrazol analogues with picrotoxin sit of the benzodiazepine-GABA receptor-inout;nophore complex. Eur J Pharmac 98:337-345.
67. Represa A, Ben-Ari Y. 1992. Kindling is associated with the formation of novel mossy fiber synapses in the CA3 region. Exp Brain Res 92:69-78.
68. Represa A, Tremblay E, Ben-Ari Y. 1987a. Kainate binding sites in the hippocampal mossy fibers: Localization and plasticity. Neuroscience 20:739-748.
69. Represa A, Tremblay E, Ben-Ari Y. 1987b. Aberrant growth of mossy fibers and enhanced kainic acid binding sites induced in rats by early hyperthyroidism. Brain Res 423:325-328.
70. Represa A, Jorquera I, Le Gal La Salle G, Ben-Ari Y. 1993. Epilepsy induced collateral sprouting of hippocampal mossy fibers: Does it induce the development of ectopic synapses with granule cell dendrites? Hippocampus 3:257-268.
71. Ribak CE, Baram TZ. 1996. Selective death of hippocampal CA3 pyramidal cells with mossy fiber afferents after CRH-induced status epilepticus in infant rats. Dev Brain Res 91:245-251.
72. Rodin EA, Schmaltz S, Twitty G. 1986. Intellectual functions of patients with childhood-onset epilepsy. Dev Med Child Neurol 28:25-33.
73. Sankar R, Wasterlain CG, and Sperber ES. 1995. Seizure-induced changes in the immature brain. In: Schwartzkroin PA, Moshé SL, Noebels JL, Swann JW, editors. Brain Development and Epilepsy. New York: Oxford University Press. p 268-288.
74. Schlessinger AR, Cowan WM, Gottlieb DI. 1975. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159:159-176.
75. Sloviter RS. 1983. "Epileptic" brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull 10:675-697.
76. Sloviter RS, Damiano BP. 1981. Sustained electrical stimulation of the perforant path duplicates kainate-induced electrophysiological effects and hippocampal damage in rats. Neurosci Lett 24:279-284.
77. Sloviter RS, Dean E, Sollas AI, Goodman JH. 1996. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol 366:516-533.
78. Sperber EF, Haas KZ, Stanton PK, Moshé SL. 1991. Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Dev Brain Res 60:88-93.
79. Sperber EF, Stanton PK, Haas K, Ackermann RF, Moshé SL. 1992. Developmental differences in the neurobiology of epileptic brain damage. In: Engel J, Jr, Wasterlain C, Cavalheiro EA, Heinemann U, Avazini G, editors. Molecular Neurobiology of Epilepsy. Amsterdam: Elsevier. p 67-81.
80. Squires RF, Saederup E, Crawley JN, Skoinick P, Paul SM. 1984. Convulsant potencies of tetrazoles are highly correlated with actions on GABA benzodiazepine picrotoxin receptor complexes in brain. Life Sci 35:1439-1444.
81. Stafstrom CE, Thompson JL, Holmes GL. 1992. Kainic acid seizures in the developing brain: Status epilepticus and spontaneous recurrent seizures. Dev Brain Res 65:227-236.
82. Stafstrom CE, Chronopoulos A, Thurber S, Thompson JL, Holmes GL. 1993. Age-dependent cognitive and behavioral deficits following kainic acid-induced seizures. Epilepsia 34:420-432.
83. Stanfield BB, Trice JE. 1988. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 72:399-406.
84. Sutula TP. 1990. Experimental models of temporal lobe epilepsy: new insights from the study of kindling and synaptic reorganization. Epilepsia Suppl. 3 31:S45-S54.
85. Sutula TP. 1993. The pathology of the epilepsies: Insights into the causes and consequences of epileptic syndromes. In: Dodson WE, Pellock JM, editors. Pediatric Epilepsy: Diagnosis and Treatment. New York: Demos Publications, p 37-44.
86. Sutula T, Xiao-Xian H, Cavazos J, Scott G. 1988. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239:1147-1150.
87. 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.
88. Sutula T, Koch J, Golarai G, Watanabe Y, McNamara JO. 1996. NMDA receptor dependence of kindling and mossy fiber sprouting: evidence that the NMDA receptor regulates patterning of hippocampal circuits in the adult brain. J Neurosci 16:7398-7406.
89. Tauck D, Nadler JV. 1985. Evidence of functional mossy fiber sprouting in the hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.
90. Thurber S, Chronopoulos A, Stafstrom CE, Holmes GL. 1992. Behavioral effects of continuous hippocampal stimulation in the developing rat. Dev Brain Res 68:35-40.
91. Thurber S, Mikati MA, Stafstrom CE, Jensen FE, Holmes GL. 1994. Quisqualic acid-induced seizures during development: A behavioral and EEG study. Epilepsia 35:868-875.
92. Van der Zee CEEM, Rashid K, Le K, Moore K-A, Stanisz J, Diamond J, Racine RJ, Fahnestock M. 1995. Intraventricular administration of antibodies to nerve growth factor retards kindling and blocks mossy fiber sprouting in adult rats. J Neurosci 15:5316-5323.
93. West JR. 1986. Long-term effects of developmental exposure to alcohol. Neurotoxicology 7:245-256.
94. West JR, Hodges CA, Black AC, Jr. 1981. Distal infrapyramidal granule cell axons possess typical mossy fiber morphology. Brain Res Bull 6:119-124.
95. West MJ. 1998. New stereological methods for counting neurons. Neurobiol Aging 14:275-285.
96. West MJ, Gundersen HJG. 1990. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1-22.
97. West MJ, Slomianka L, Gundersen HJG. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
98. Wimer C, Wimer RE, Wimer JS. 1983. An association between granule cell density in the dentate gyrus and two-way avoidance conditioning in the house mouse. Behav Neurosci 97:844-856.
99. Wuarin J-P, Dudek EF. 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.
100. Yang Y, Tandon P, Liu Z, Sarkisian MR, Stafstrom CE, Holmes GL. 1998. Synaptic reorganization following kainic acid-induced seizures during development. Dev Brain Res 107:169-177.