Neonatal exposure to low-dose domoic acid lowers seizure threshold in adult rats

Neuroscience

Volumn 169, Issue 4, 2010, Pages 1789-1799

  Gill, D A ^a   Bastlund, J F ^b   Watson, W P ^b   Ryan, C L ^a   Reynolds, D S ^b   Tasker, R A ^a  

^a UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

^b H LUNDBECK A S   (Denmark)

Author keywords

Developmental rat model; Epilepsy; Kindling; Mossy fibre sprouting; Radio telemetry

Indexed keywords

DOMOIC ACID; PENTETRAZOLE;

AFTERDISCHARGE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CONVULSION; DENTATE GYRUS; ELECTROENCEPHALOGRAM; FOCAL EPILEPSY; GRAND MAL SEIZURE; KINDLING; LATENT PERIOD; MALE; MOSSY FIBER; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; SEIZURE THRESHOLD; TONIC CLONIC SEIZURE;

EID: 77955413501     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.06.045     Document Type: Article

References (68)

1. Adams B., Lee M., Fahnestock M., Racine R.J. Long-term potentiation trains induce mossy fibre sprouting. Brain Res 1997, 775:193-197.
2. Andre V., Pineau N., Motte J.E., Marescaux C., Nehlig A. Mapping of neuronal networks underlying generalized seizures induced by increasing doses of pentylenetetrazol in the immature and adult rat: a c-Fos immunohistochemical study. Eur J Neurosci 1998, 10:2094-2106.
3. Armitage L.L., Mohapel P., Jenkins E.M., Hannesson D.K., Corcoran M.E. Dissociation between mossy fiber sprouting and rapid kindling with low-frequency stimulation of the amygdala. Brain Res 1998, 781:37-44.
4. Arrieta O., Palencia G., Garc¡a-Arenas G., Morales-Espinosa D., Hernandez-Pedro N., Sotelo J. Prolonged exposure to lead lowers the threshold of pentylenetetrazole-induced seizures in rats. Epilepsia 2005, 46:1599-1602.
5. Bastlund J.F., Jennum P., Mohapel P., Penschuck S., Watson W.P. Spontaneous epileptic rats show changes in sleep architecture and hypothalamic pathology. Epilepsia 2005, 46:934-938.
6. Bastlund J.F., Jennum P., Mohapel P., Vogel V., Watson W.P. Measurement of cortical and hippocampal epileptiform activity in freely moving rats by means of implantable radiotelemetry. J Neurosci Methods 2004, 138:65-72.
7. Bausch S.B. Potential roles for hyaluronan and CD44 in kainic acid-induced mossy fiber sprouting in organotypic hippocampal slice cultures. Neuroscience 2006, 143:339-350.
8. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev 2002, 3:728-739.
9. Bernard P.B., Macdonald D.S., Gill D.A., Ryan C.L., Tasker R.A. Hippocampal mossy fiber sprouting and elevated trkB receptor expression following systemic administration of low dose domoic acid during neonatal development. Hippocampus 2007, 17:1121-1133.
10. Blume W.T. The progression of epilepsy. Epilepsia 2006, 47(Suppl 1):71-78.
11. Bonan C.D., Amaral O.B., Rockenback I.C., Walz R., Battastini A.M.O., Izquierdo I., Sarkis J.J.F. Altered ATP hydrolysis induced by pentylenetetrazol kindling in rat brain synaptosomes. Neurochem Res 2000, 25:775-779.
12. Brooks-Kayal A.R. Rearranging receptors. Epilepsia 2005, 46(Suppl 7):29-38.
13. Burgard E.C., Hablitz J.J. Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. J Neurophysiol 1993, 69:230-239.
14. Dakshinamurti K., Sharma S.K., Sundaram M., Watanabe T. Hippocampal changes in developing postnatal mice following intrauterine exposure to domoic acid. J Neurosci 1993, 13:4486-4495.
15. Dobbing J., Smart J.L. Vulnerability of developing brain and behaviour. Br Med Bull 1974, 30:164-168.
16. Doucette T.A., Strain S.M., Allen G.V., Ryan C.L., Tasker R.A.R. Comparative behavioural toxicity of domoic acid and kainic acid in neonatal rats. Neurotoxicol Teratol 2000, 22:862-869.
17. Doucette T.A., Bernard P.B., Yuill P.C., Tasker R.A., Ryan C.L. Low doses of non-NMDA glutamate receptor agonists alter neurobehavioural development in the rat. Neurotoxicol Teratol 2003, 25:473-479.
18. Doucette T.A., Bernard P.B., Husum H., Perry M.A., Ryan C.L., Tasker R.A. Low doses of domoic acid during postnatal development produce permanent changes in rat behaviour and hippocampal morphology. Neurotox Res 2004, 6:555-563.
19. Doucette T.A., Ryan C.L., Tasker R.A. Gender-based changes in cognition and emotionality in a new rat model of epilepsy. Amino Acids 2007, 32:317-322.
20. Duchowny M.S., Burchfiel J.L. Facilitation and antagonism of kindled seizure development in the limbic system of the rat. Electroencephalogr Clin Neurophysiol 1981, 51:403-416.
21. Flynn C., Teskey G.C. Reduction of seizure thresholds following electrical stimulation of sensorimotor cortex is dependent on stimulation intensity and is not related to synaptic potentiation. Neuroscience 2007, 149:263-272.
22. Galic M.A., Riazi K., Heida J.G., Mouihate A., Fournier N.M., Spencer S.J., Kalynchuk L.E., Teskey G.C., Pittman Q.J. Postnatal inflammation increases seizure susceptibility in adult rats. J Neurosci 2008, 28:6904-6913.
23. Galvan C.D., Hrachovy R.A., Smith K.L., Swann J.W. Blockade of neuronal activity during hippocampal development produces a chronic focal epilepsy in the rat. J Neurosci 2000, 20:2904-2916.
24. Goddard G.V. Development of epileptic seizures through brain stimulation at low intensity. Nature 1967, 214:1020-1021.
25. Haas K.Z., Sperber E.F., Moshe S.L. Kindling in developing animals: interactions between ipsilateral foci. Brain Res Dev Brain Res 1992, 68:140-143.
26. Haas K.Z., Sperber E.F., Moshe S.L. Kindling in developing animals: expression of severe seizures and enhanced development of bilateral foci. Brain Res Dev Brain Res 1990, 56:275-280.
27. Hassan H., Pohle W., Rüthrich H., Brödemann R., Krug M. Repeated long-term potentiation induces mossy fibre sprouting and changes the sensibility of hippocampal granule cells to subconvulsive doses of pentylenetetrazol. Eur J Neurosci 2000, 12:1509-1515.
28. Hewapathirane D.S., Burnham W.M. Propagation of amygdala-kindled seizures to the hippocampus in the rat: electroencephalographic features and behavioural correlates. Neurosci Res 2005, 53:369-375.
29. Holahan M.R., Rekart J.L., Sandoval J., Routtenberg A. Spatial learning induces presynaptic structural remodeling in the hippocampal mossy fibre system of two rat strains. Hippocampus 2006, 16:560-570.
30. 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, 404:537-553.
31. Hougaard K.A., Andersen M.B., Kjær S.L., Hansen M., Werge T., Lund S.P. Prenatal stress may increase vulnerability to life events: comparison with the effects of prenatal dexamethasone. Brain Res Dev Brain Res 2005, 159:55-63.
32. Kirkby R.D., Gilbert T.H., Corcoran M.E. Kindling antagonism: mapping of susceptible sites. Brain Res 1993, 616:17-24.
33. Kirkby R.D., Gilbert T.H., Westcott M.C., Corcoran M.E. Further characterization of kindling antagonism. Epilepsy Res 1995, 21:115-124.
34. Klass D.W. Electroencephalographic manifestations of complex partial seizures. Adv Neurol 1975, 11:113-140.
35. Leite J.P., Babb T.L., Pretorius J.K., Kuhlman P.A., Yeoman K.M., Mathern G.W. Neuron loss, mossy fiber sprouting, and interictal spikes after intrahippocampal kainate in developing rats. Epilepy Res 1996, 26:219-231.
36. Levin E.D., Pizarro K., Pang W.G., Harrison J., Ramsdell J.S. Persisting behavioral consequences of prenatal domoic acid exposure in rats. Neurotoxicol Teratol 2005, 27:719-725.
37. McIntyre D.C. The kindling phenomenon. Models of Seizure and epilepsy 2006, 351-363. Elsevier Academic, Burlington, MA. A. Pitkanen, P.A. Schwartzkroin, S.L. Moshe (Eds.).
38. McIntyre D.C., Gilby K.L. Mapping seizure pathways in the temporal lobe. Epilepsia 2008, 49(Suppl 3):23-30.
39. Moshe S.L., Albala B.J. Maturational changes in postictal refractoriness and seizure susceptibility in developing rats. Ann Neurol 1983, 13:552-557.
40. Moshe S.L., Albala B.J., Ackermann R.F., Engel J. Increased seizure susceptibility of the immature brain. Brain Res 1983, 283:81-85.
41. Nakajima S., Potvin J.L. Neural and behavioural effects of domoic acid, an amnesic shellfish toxin, in the rat. Can J Psychol 1992, 46:569-581.
42. Nouws J.F.M. Pharmacokinetics in immature animals: a review. J Anim Sci 1992, 70:3627-3634.
43. Novelli A., Fernandez-Sanchez M.T., Doucette T.A., Tasker R.A.R. Chemical and biological detection methods. Seafood and freshwater toxins 2000, 383-399. Marcel Dekker, New York, NY. L.M. Botana (Ed.).
44. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Elsevier, San Diego, CA.
45. Perry M.A., Ryan C.L., Tasker R.A. Effects of low dose neonatal domoic acid administration on behavioural and physiological response to mild stress in adult rats. Physiol Behav 2009, 98:53-59.
46. Porter B.E. Neurogenesis and epilepsy in the developing brain. Epilepsia 2008, 49(Suppl 5):50-54.
47. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972, 32:281-294.
48. Ramirez-Amaya V., Escobar M.L., Chao V., Bermudez-Rattoni F. Synaptogenesis of mossy fibres induced by spatial water maze overtraining. Hippocampus 1999, 9:631-636.
49. Ramirez-Amaya V., Balderas I., Sandoval J., Escobar M.L., Bermudez-Rattoni F. Spatial long-term memory is related to mossy fibre synaptogenesis. J Neurosci 2001, 21:7340-7348.
50. Represa A., Ben-Ari Y. Kindling is associated with the formation of novel mossy fibre synapses in the CA3 region. Exp Brain Res 1992, 92:69-78.
51. Santos N.F., Correia M.L., Sinigaglia-Coimbra R., Calderazzo L., Sanabria E.R.G., Cavalheiro E.A. Multiple pilocarpine-induced status epilepticus in developing rats; A long-term behavioral and electrophysiological study. Epilepsia 2000, 41:S57-S63.
52. Schmoll H., Badan I., Grecksch G., Walker L., Kessler C., Popa-Wagner A. Kindling status in sprague-dawley rats induced by pentylenetetrazole. Am J Pathol 2003, 162:1027-1034.
53. Sommer B., Burnashev N., Verdoorn T.A., Keinänen K., Sakmann B., Seeburg P.H. A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 1992, 11:1651-1656.
54. Sperber E.F., Haas K.Z., Stanton P.K., Moshe S.L. Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Brain Res Dev Brain Res 1991, 60:8-93.
55. Stafstrom C.E., Sutula T.P. Models of epilepsy in the developing and adult brain: implications for neuroprotection. Epilepsy Behav 2005, 7(Suppl 3):S18-S24.
56. Stafstrom C.E., Thompson J.L., Holmes G.L. Kainic acid seizures in the developing brain: Status epilepticus and spontaneous recurrent seizures. Brain Res Dev Brain Res 1992, 65:227-236.
57. Sutula T. Seizure-induced axonal sprouting: assessing connections between injury, local circuits, and epileptogenesis. Epilepsy Curr 2002, 2:86-91.
58. Sutula T., He X.X., Cavazos J., Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 1988, 239:1147-1150.
59. Sutula T.P., Dudek F.E. Unmasking recurrent excitation generated by mossy fibre sprouting in the epileptic dentate gyrus: an emergent property of a complex system. Prog Brain Res 2007, 163:541-563.
60. Tasker R.A., Strain S.M., Drejer J. Selective reduction in domoic acid toxicity in vivo by a novel non-N-methyl-D-aspartate receptor antagonist. Can J Physiol Pharmacol 1996, 74:1047-1054.
61. Tasker R.A., Connell B.J., Strain S.M. Pharmacology of systemically administered domoic acid in mice. Can J Physiol Pharmacol 1991, 69:378-382.
62. Tasker R.A.R., Perry M.A., Doucette T.A., Ryan C.L. NMDA receptor involvement in the effects of low dose domoic acid in neonatal rats. Amino Acids 2005, 28:193-196.
63. Tiedeken J.A., Ramsdell J.S. Embryonic exposure to domoic acid increases the susceptibility of zebrafish larvae to the chemical convulsant pentylenetetrazole. Environ Health Perspect 2007, 115:1547-1552.
64. Tyzio R., Represa A., Jorquera I., Ben-Ari Y., Gozlan H., Aniksztejn L. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J Neurosci 1999, 19:10372-10382.
65. Verdoorn T.A., Johansen T.H., Drejer J., Nielsen E.O. Selective block of recombinant glur6 receptors by NS-102, a novel non-NMDA receptor antagonist. Eur J Pharmacol 1994, 269:43-49.
66. Williams P., White A., Ferraro D., Clark S., Staley K., Dudek F.E. The use of radiotelemetry to evaluate electrographic seizures in rats with kainate-induced epilepsy. J Neurosci Methods 2006, 155:39-48.
67. Zhang G., Raol Y.S., Hsu F.C., Brooks-Kayal A.R. Long-term alterations in glutamate receptor and transporter expression following early-life seizures are associated with increased seizure susceptibility. J Neurochem 2004, 88:91-101.
68. Zhang X., Shu-Sen C., Wallace A.E., Hannesson D.K., Schmued L.C., Saucier D.M., Honer W.G., Corcoran M.E. Relations between brain pathology and temporal lobe epilepsy. J Neurosci 2002, 22:6052-6061.