Persistent changes in learning and memory in rats following neonatal treatment with domoic acid

Physiology and Behavior

Volumn 96, Issue 4-5, 2009, Pages 505-512

  Adams, Amber L ^a   Doucette, Tracy A ^a   James, Rebecca ^a   Ryan, Catherine L ^a  

^a UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

Author keywords

Development; Domoic acid; Glutamate; Kainate receptors; Morris Water Maze; Radial arm maze; Rat; Spatial learning

Indexed keywords

DOMOIC ACID; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR AGONIST; KAINIC ACID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN MATURATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; LEARNING; LOW DRUG DOSE; MALE; MAZE TEST; MEMORY; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CRITICAL PERIOD (PSYCHOLOGY); ESCAPE REACTION; EXCITATORY AMINO ACID AGONISTS; FEMALE; HIPPOCAMPUS; KAINIC ACID; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MENTAL RECALL; NEUROTOXINS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SPATIAL BEHAVIOR;

EID: 60249087103     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2008.11.019     Document Type: Article

References (63)

1. McDonald J.W., and Johnston M.V. Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Brain Res Rev 15 (1990) 41-70
2. Olney J.W., and Ishimaru M.J. Excitotoxic cell death. In: Koliatsos V.E., and Ratan R.R. (Eds). Cell death and diseases of the nervous system (1999), Humana Press, Totowa, N.J.
3. Rice D., and Barone Jr. S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108 (2000) 511-533 Suppl 3
4. Vorhees C.V. Principles of behavioral teratology. In: Riley E.P., and Vorhees C.V. (Eds). Handbook of behavioral teratology (1986), Plenum Press, New York 23-48
5. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 3 (1979) 79-83
6. Dobbing J. Vulnerable periods in brain growth and somatic growth. In: Roberts D.F., and Thomson A.M. (Eds). The biology of human fetal growth (1976), Taylor and Francis, London 137-147
7. Dobbing J., and Smart J.L. Vulnerability of developing brain and behaviour. Br Med Bull 30 (1974) 164-168
8. McDonald J.W., and Johnston M.V. Excitatory amino acid neurotoxicity in the developing brain. NIDA Res Monogr 133 (1993) 185-205
9. Ozawa S., Kamiya H., and Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54 (1998) 581-618
10. Rison R.A., and Stanton P.K. Long-term potentiation and N-Methyl-d-aspartate receptors: foundations of memory and neurologic disease?. Neurosci Biobehav Rev 19 (1995) 533-552
11. Collingridge G.L., and Singer W. Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci 11 (1990) 290-296
12. Frerking M., Schmitz D., Zhou Q., Johansen J., and Nicoll R.A. Kainate receptors depress excitatory synaptic transmission at CA3-CA1 synapses in the hippocampus via a direct presynaptic action. J Neurosci 21 (2001) 2958-2966
13. Ben-Ari Y., and Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23 (2000) 580-587
14. Reid C.A., and Bliss T.V. Learning about kainate receptors. Trends Pharmacol Sci 21 (2000) 159-160
15. Bleakman D., and Lodge D. Neuropharmacology of AMPA and kainate receptors. Neuropharmacol 37 (1998) 1187-1204
16. Grigorenko E.V., Bell W.L., Glazier S., Pons T., and Deadwyler S. Editing status at the Q/R site of the GluR2 and GluR6 glutamate receptor subunits in the surgically excised hippocampus of patients with refractory epilepsy. Neuroreport 9 (1998) 2219-2224
17. Mulle C., Sailer A., Perez-Otano I., Dickinson-Anson H., Castillo P.E., Bureau I., et al. Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392 (1998) 601-605
18. Grigorenko E., Glazier S., Bell W., Tytell M., Nosel E., Pons T., et al. Changes in glutamate receptor subunit composition in hippocampus and cortex in patients with refractory epilepsy. J Neurol Sci 153 (1997) 35-45
19. Bortolotto Z.A., Clarke V.R.J., Delany C.M., Parry M.C., Smolders I., Vignes M., et al. Kainate receptors are involved in synaptic plasticity. Nature 402 (1999) 297-301
20. Bortolotto Z.A., Nistico R., More J.C., and Jane DE Collingridge G.L. Kainate receptors and mossy fiber LTP. Neurotoxicology 26 (2005) 769-777
21. Wisden W., Seeburg P.H., and Monyer H. AMPA, kainate and NMDA ionotropic glutamate receptor expression: an in situ hybridization atlas. In: Otterson O.P., and Storm-Mathisen J. (Eds). Handbook of chemical neuroanatomy vol. 18 (2000), Elsevier, New York 99-143
22. McDonald R.J., and White N.M. Hippocampal and nonhippocampal contributions to place learning in rats. Behav Neurosci 109 (1995) 579-593
23. McNamara R.K., and Skelton R.W. The neuropharmacological and neurochemical basis of place learning in the Morris Water Maze. Brain Res Brain Res Rev 18 (1993) 33-49
24. Eichenbaum H., Stewart C., and Morris R.G. Hippocampal representation in place learning. J Neurosci 10 (1990) 3531-3542
25. Bubeníková-Valešová V., Balcar V., Tejkalová H., Langmeier M., and Št'astný F. Neonatal administration of N-acetly-l-aspartyl-l-glutamate induces early neurodegeneration in hippocampus and alters behaviour in young adult rats. Neurochem Int 48 (2006) 515-522
26. Hunt S. Neonatal treatment with a competitive NMDA antagonist results in response-specific disruption of conditioned fear in preweanling rats. Psychopharmacology 185 (2006) 179-187
27. Stefani M.R., and Moghaddam B. Transient N-methyl-d-aspartate recsptor blockade in early development causes lasting cognitive deficits relevant to schizophrenia. Biol Psychiatry 57 (2005) 433-436
28. Stafstrom C.E., and Sasaki-Adams D.M. NMDA-induced seizures in developing rats cause long-term learning impairment and increased seizure susceptibility. Epilepsy Res 53 (2003) 12129-12138
29. Wangen K., Myhrer T., Moldstad J.N., Iversen E.G., and Fonnum F. Modulatory treatment of NMDA receptors in neonatal rats affects cognitive behavior in adult age. Dev Brain Res 99 (1997) 126-130
30. Ritter L.M., Vazquez D.M., and Meador-Woodruff J.H. Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res Dev Brain Res 139 (2002) 227-236
31. Vissel B., Royle G.A., Christie B.R., Schiffer H.H., Ghetti A., Tritto T., et al. The role of RNA editing of kainate receptors in synaptic plasticity. Neuron 29 (2001) 217-227
32. Bernard A., Ferhat L., Charton G., Represa A., Ben-Ari Y., and Khrestchatisky M. Q/R editing of the rat GluR5 and GluR6 kainate receptors in vivo and in vitro: evidence for independent development, pathological and cellular regulation. Eur J Neurosci 11 (1999) 604-616
33. Paschen W., Schmitt J., Gissel C., and Dux E. Developmental changes of RNA editing of glutamate receptor subunits GluR5 and GluR6: in vivo versus in vitro. Brain Res Dev Brain Res 98 (1997) 271-280
34. Bernard A., and Khrestchatisky M. Assessing the extent of RNA editing in the TMII regions of GluR5 and GluR6 kainate receptors during rat brain development. J Neurochem 62 (1994) 2057-2060
35. Schmitt J., Dux E., Gissel C., and Paschen W. Regional analysis of developmental changes in the extent of GluR6 mRNA editing in rat brain. Brain Res Dev Brain Res 91 (1996) 153-157
36. Egebjerg J., and Heinemann S.F. Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci U S A 90 (1993) 755-759
37. Kohler M., Burnashev N., Sakmann B., and Seeburg P.H. Determinants of calcium permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 10 (1993) 491-500
38. Hume R.I., Dingledine R., and Heinemann S.F. Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 253 (1991) 1028-1031
39. Monyer H., Seeburg P.H., and Wisden W. Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 6 (1991) 799-810
40. Sommer B., Kohler M., Sprengel R., and Seeburg P.H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67 (1991) 11-19
41. Verdoorn T.A., Johansen T.H., Drejer J., and Nielsen E.O. Selective block of recombinant GluR6 receptors by NS-102, a novel non-NMDA receptor antagonist. Eur J Pharmacol 269 (1994) 43-49
42. Kaufmann W. Developmental neurotoxicity. In: Krinke G.J. (Ed). The handbook of experimental animals: the laboratory rat (2000), Academic Press, New York 227-252
43. Levin E.D., Pizarro K., Pang W.G., Harrison J., and Ramsdell J.S. Persisting behavioral consequences of prenatal domoic acid exposure in rats. Neurotoxicol Teratol 27 5 (2005) 719-725
44. Levin E.D., Pang W.G., Harrison J., Williams P., Petro A., and Ramsdell J.S. Persistent neurobehavioral effects of early postnatal domoic acid exposure in rats. Neurotoxicol Teratol 28 6 (2006) 673-680
45. Doucette T.A., Bernard P.B., Yuill P.C., and Tasker RA Ryan C.L. Low doses of non-NMDA glutamate receptor agonists alter neurobehavioural development in the rat. Neurotoxicol Teratol 25 (2003) 473-479
46. Doucette T.A., Bernard P.B., Husum H., Perry M.A., Ryan C.L., and Tasker R.A.R. Low doses of domoic acid during postnatal development produce permanent changes in rat behaviour and hippocampal morphology. Neurotox Res 6 (2004) 555-563
47. Tasker R.A.R., Perry M.A., Doucette T.A., and Ryan C.L. NMDA receptor involvement in the effects of low dose domoic acid in neonatal rats. Amino Acids 28 (2005) 193-196
48. Doucette T.A., Ryan C.L., and Tasker R.A. Gender-based changes in cognition and emotionality in a new rat model of epilepsy. Amino Acids 32 (2007) 317-322
49. Bernard P., MacDonald D., Gill D., Ryan C.L., and Tasker R.A.R. Hippocampal mossy fibre sprouting and elevated trkB receptor expression following systemic administration of low dose domoic acid during neonatal development. Hippocampus 17 11 (2007) 1121-1133
50. Burt M.A., and Ryan CL Doucette T.A. Low dose domoic acid in neonatal rats abolishes nicotine induced place preference during late adolescence. Amino Acids 35 1 (2008) 247-249
51. Burt M.A., Ryan C.L., and Doucette T.A. Altered responses to novelty and drug reinforcement in adult rats treated neonatally with domoic acid. Physiol Behav 93 (2008) 327-336
52. Adams A.L., Doucette T.A., and Ryan C.L. Altered pre-pulse inhibition in adult rats treated neonatally with domoic acid. Amino Acids 35 1 (2008) 157-160
53. Paxinos G., Tork I., Tecott L.H., and Valentino K.L. Atlas of the developing rat brain (1991), Academic Press, San Diego
54. Chambers R.A., Moore J., McEvoy J.P., and Levin E.D. Cognitive effects of neonatal hippocampal lesions in a rat model of schizophrenia. Neuropsychopharmacology 15 6 (1996) 587-594
55. Morris R.G.M. Spatial localization does not require the presence of local cues. Learn Motiv 12 (1981) 239-260
56. Schwegler H., Crusio W.E., and Brust I. Correlations between radial-maze learning and structural variations of septum and hippocampus in rodents. Behav Brain Res 67 (1995) 29-41
57. Schwegler H., Mueller G.G., Crusio W.E., Szemes L., and Seress L. Hippocampal morphology and spatially related behavior in Long-Evans and CFY rats. Hippocampus 3 (1993) 1-8
58. Prior H., Schwegler H., and Dücker G. Dissociation of spatial reference memory, spatial working memory, and hippocampal mossy fiber distribution in two rat strains differing in emotionality. Behav Brain Res 87 (1997) 183-194
59. Sava S., and Marcus E.J. Intramaze cue utilization in the water maze: effects of sex and estrous cycle in rats. Horm Behav 48 1 (2005) 23-33
60. Gengler S., Mallot H.A., and Hölscher C. Inactivation of the rat dorsal striatum impairs performance in spatial tasks and alters hippocampal theta in the freely moving rat. Behav Brain Res 164 1 (2005) 73-82
61. Compton D.M., Griffith H.R., McDaniel W.F., Foster R.A., and Davis B.K. The flexible use of multiple cue relationships in spatial navigation: a comparison of water maze performance following hippocampal, medial septal, prefrontal cortex, or posterior parietal cortex lesions. Neurobiol Learn Mem 68 2 (1997) 117-132
62. de Bruin J.P., Swinkels W.A., and de Brabander J.M. Response learning of rats in a Morris Water Maze: involvement of the medical prefrontal cortex. Behav Brain Res 85 1 (1997) 47-55
63. Tait D.S., and Brown V.J. Difficulty overcoming learned non-reward during reversal learning in rats with ibotenic acid lesions of orbital prefrontal cortex. Ann NY Acad Sci 1121 (2007) 407-420