Low-dose neonatal domoic acid causes persistent changes in behavioural and molecular indicators of stress response in rats

Behavioural Brain Research

Volumn 230, Issue 2, 2012, Pages 409-417

  Gill, Daphne A ^a   Perry, Melissa A ^a   McGuire, Emily P ^a   Pérez Gómez, Anabel ^a   Tasker, R Andrew ^a  

^a UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

Author keywords

Anxiety; Corticosteroid receptors; Epilepsy; Neurodevelopmental disorders; Perseverance

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; ALPHA 2C ADRENERGIC RECEPTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; DOMOIC ACID; DOPAMINE 2 RECEPTOR; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MINERALOCORTICOID; MINERALOCORTICOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR DISORDER; COGNITION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; FEMALE; FORCED SWIMMING TEST; MALADJUSTMENT; MALE; MAZE TEST; NEWBORN; NONHUMAN; PERSEVERATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEIZURE; SEX DIFFERENCE; STRESS; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; FEMALE; KAINIC ACID; MALE; NEUROTOXINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECEPTORS, DOPAMINE D2; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; RECEPTORS, STEROID; SEIZURES; SEX FACTORS; STRESS, PSYCHOLOGICAL;

EID: 84859269078     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.02.036     Document Type: Article

References (73)

1. Dobbing J., Smart J.L. Vulnerability of developing brain and behaviour. Br Med Bull 1974, 30:164-168.
2. Nouws J.F.M. Pharmacokinetics in immature animals: a review. J Anim Sci 1992, 70:3627-3634.
3. Adams A.L., Doucette T.A., Ryan C.L. Altered pre-pulse inhibition in adult rats treated neonatally with domoic acid. Amino Acids 2008, 35:157-160. 10.1007/s00726-007-0603-3.
4. Adams A.L., Doucette T.A., James R., Ryan C.L. Persistent changes in learning and memory in rats following neonatal treatment with domoic acid. Physiol Behav 2009, 96:505-512. 10.1016/j.physbeh.2008.11.019.
5. Burt M.A., Ryan C.L., Doucette T.A. Altered responses to novelty and drug reinforcement in adult rats treated neonatally with domoic acid. Physiol Behav 2008, 93:327-336. 10.1016/j.physbeh.2007.09.003.
6. Burt M.A., Ryan C.L., Doucette T.A. Low dose domoic acid in neonatal rats abolishes nicotine induced conditioned place preference during late adolescence. Amino Acids 2008, 35:247-249. 10.1007/s00726-007-0584-2.
7. 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. 10.1007/s00726-006-0418-7.
8. 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.
9. 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. 10.1016/j.physbeh.2009.04.009.
10. 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. 10.1002/hipo.20342.
11. Gill D.A., Bastlund J.F., Watson W.P., Ryan C.L., Reynolds D.S., Tasker R.A. Neonatal exposure to low-dose domoic acid lowers seizure threshold in adult rats. Neuroscience 2010, 169:1789-1799. 10.1016/j.neuroscience.2010.06.045.
12. Gill D.A., Bastlund J.F., Anderson N.J., Tasker R.A. Reductions in paradoxical sleep time in adult rats treated neonatally with low dose domoic acid. Behav Brain Res 2009, 205:564-567. 10.1016/j.bbr.2009.07.018.
13. Gill D.A., Ramsay S.L., Tasker R.A. Selective reductions in subpopulations of GABAergic neurons in a developmental rat model of epilepsy. Brain Res 2010, 1331:114-123. 10.1016/j.brainres.2010.03.054.
14. Frucht M.M., Quigg M., Schwaner C., Fountain N.B. Distribution of seizure precipitants among epilepsy syndromes. Epilepsia 2000, 41:1534-1539.
15. Nakken K.O., Solaas M.H., Kjeldsen M.J., Friis M.L., Pellock J.M., Corey L.A. Which seizure-precipitating factors do patients with epilepsy most frequently report?. Epilepsy Behav 2005, 6:85-89. 10.1016/j.yebeh.2004.11.003.
16. Pinikahana J., Dono J. The lived experience of initial symptoms of and factors triggering epileptic seizures. Epilepsy Behav 2009, 15:513-520. 10.1016/j.yebeh.2009.06.004.
17. Temkin N.R., Davis G.R. Stress as a risk factor for seizures among adults with epilepsy. Epilepsia 1984, 25:450-456.
18. Joels M., Baram T.Z. The neuro-symphony of stress. Nat Rev Neurosci 2009, 10:459-466. 10.1038/nrn2632.
19. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009, 10:434-445. 10.1038/nrn2639.
20. Koe A.S., Jones N.C., Salzberg MR Early life stress as an influence on limbic epilepsy: an hypothesis whose time has come?. Front Behav Neurosci 2009, 3:24. 10.3389/neuro.08.024.2009.
21. Joels M. Functional actions of corticosteroids in the hippocampus. Eur J Pharmacol 2008, 583:312-321. 10.1016/j.ejphar.2007.11.064.
22. Howland J.G., Wang Y.T. Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res 2008, 169:145-158. 10.1016/S0079-6123(07)00008-8.
23. Simon A.B., Gorman J.M. Advances in the treatment of anxiety: targeting glutamate. NeuroRx 2006, 3:57-68. 10.1016/j.nurx.2005.12.005.
24. Zarate C., Machado-Vieira R., Henter I., Ibrahim L., Diazgranados N., Salvadore G. Glutamatergic modulators: the future of treating mood disorders?. Harv Rev Psychiatry 2010, 18:293-303. 10.3109/10673229.2010.511059.
25. Hunter R.G., Bellani R., Bloss E., Costa A., McCarthy K., McEwen BS Regulation of kainate receptor subunit mRNA by stress and corticosteroids in the rat hippocampus. PLoS One 2009, 4:e4328. 10.1371/journal.pone.0004328.
26. Debonnel G., Weiss M., de Montigny C Neurotoxic effect of domoic acid: mediation by kainate receptor electrophysiological studies in the rat. Can Dis Wkly Rep 1990, 16(Suppl 1E):59-68.
27. Lomeli H., Wisden W., Kohler M., Keinanen K., Sommer B., Seeburg P.H. High-affinity kainate and domoate receptors in rat brain. FEBS Lett 1992, 307:139-143.
28. 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.
29. 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.
30. 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.
31. Hsu F.C., Zhang G.J., Raol Y.S., Valentino R.J., Coulter D.A., Brooks-Kayal A.R. Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses. Proc Natl Acad Sci U S A 2003, 100:12213-12218. 10.1073/pnas.2131679100.
32. Racine R.J. Modification of seizure activity by electrical brain stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972, 32:281-294.
33. Ahmed T., Frey J.U., Korz V. Long-term effects of brief acute stress on cellular signaling and hippocampal LTP. J Neurosci 2006, 26:3951-3958. 10.1523/JNEUROSCI.4901-05.2006.
34. Kalman B.A., Spencer R.L. Rapid corticosteroid-dependent regulation of mineralocorticoid receptor protein expression in rat brain. Endocrinology 2002, 143:4184-4195.
35. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
36. Gill D.A., Bastlund J.F., Reynolds D.S., Watson W.P., Ryan C.L., Tasker RA Perinatal exposure to low-dose domoic acid produces altered EEG patterns and reduced seizure threshold in the adult rat. Proceedings of the 36th Annual Meeting of the Society for Neuroscience 2006, abstract # 280.5.
37. Ryan C.L., Robbins M.A., Smith M.T., Gallant I.C., Adams-Marriott A.L., Doucette T.A. Altered social interaction in adult rats following neonatal treatment with domoic acid. Physiol Behav 2011, 102:291-295. 10.1016/j.physbeh.2010.11.020.
38. Kwak H.R., Lee J.W., Kwon K.J., Kang C.D., Cheong I.Y., Chun W., et al. Maternal social separation of adolescent rats induces hyperactivity and anxiolytic behavior. Korean J Physiol Pharmacol 2009, 13:79-83. 10.4196/kjpp.2009.13.2.79.
39. Fernandes C., Gonzalez M.I., Wilson C.A., File S.E. Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav 1999, 64:731-738.
40. Carobrez A.P., Bertoglio L.J. Ethological temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29:1193-1205. 10.1016/j.neubiorev.2005.04.017.
41. Rodgers R.J., Dalvi A. Anxiety, defence and the elevated plus-maze. Neurosci Biobehav Rev 1997, 21:801-810.
42. Bourke C.H., Neigh G.N. Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic. Horm Behav 2011, 10.1016/j.yhbeh.2011.03.011.
43. McLaughlin K.J., Baran S.E., Conrad C.D. Chronic stress- and sex-specific neuromorphological and functional changes in limbic structures. Mol Neurobiol 2009, 40:166-182. 10.1007/s12035-009-8079-7.
44. Brunton P.J., Russell J.A. Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects. J Neuroendocrinol 2010, 22:258-271. 10.1111/j.1365-2826.2010.01969.x.
45. Karandrea D., Kittas C., Kitraki E. Forced swimming differentially affects male and female brain corticosteroid receptors. Neuroendocrinology 2002, 75:217-226.
46. Bowman R.E. Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan. J Neuroendocrinol 2005, 17:526-535. 10.1111/j.1365-2826.2005.01335.x.
47. Philipp M., Brede M., Hein L. Physiological significance of alpha(2)-adrenergic receptor subtype diversity: one receptor is not enough. Am J Physiol Regul Integr Comp Physiol 2002, 283:R287-R295. 10.1152/ajpregu.00123.2002.
48. Sallinen J., Haapalinna A., MacDonald E., Viitamaa T., Lahdesmaki J., Rybnikova E., et al. Genetic alteration of the alpha2-adrenoceptor subtype c in mice affects the development of behavioral despair and stress-induced increases in plasma corticosterone levels. Mol Psychiatry 1999, 4:443-452.
49. Laarakker M.C., Raai J.R., van Lith H.A., Ohl F. The role of the alpha 2A-adrenoceptor in mouse stress-coping behaviour. Psychoneuroendocrinology 2010, 35:490-502. 10.1016/j.psyneuen.2009.08.014.
50. Kim J.J., Song E.Y., Kosten T.A. Stress effects in the hippocampus: synaptic plasticity and memory. Stress 2006, 9:1-11. 10.1080/10253890600678004.
51. Morgane P.J., Galler J.R., Mokler D.J. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol 2005, 75:143-160. 10.1016/j.pneurobio.2005.01.001.
52. Bertram E.H., Zhang D.X., Mangan P., Fountain N., Rempe D. Functional anatomy of limbic epilepsy: a proposal for central synchronization of a diffusely hyperexcitable network. Epilepsy Res 1998, 32:194-205. 10.1016/S0920-1211(98)00051-5.
53. Karst H., Berger S., Turiault M., Tronche F., Schutz G., Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci U S A 2005, 102:19204-19207. 10.1073/pnas.0507572102.
54. Olijslagers J.E., de Kloet E.R., Elgersma Y., van Woerden G.M., Joels M., Karst H. Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci 2008, 27:2542-2550. 10.1111/j.1460-9568.2008.06220.x.
55. de Kloet E.R., Karst H., Joels M. Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 2008, 29:268-272. 10.1016/j.yfrne.2007.10.002.
56. Tasker J.G., Di S., Malcher-Lopes R. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 2006, 147:5549-5556. 10.1210/en.2006-0981.
57. Joels M., Karst H., DeRijk R., de Kloet E.R. The coming out of the brain mineralocorticoid receptor. Trends Neurosci 2008, 31:1-7. 10.1016/j.tins.2007.10.005.
58. Hwang I.K., Lee Y.B., Yoo K.Y., Kang T.C., Kim D.W., Moon W.K., et al. Seizure-induced changes of mineralocorticoid and glucocorticoid receptors in the hippocampus in seizure sensitive gerbils. Neurosci Res 2005, 53:14-24. 10.1016/j.neures.2005.05.006.
59. Cahill L. Why sex matters for neuroscience. Nat Rev Neurosci 2006, 7:477-484. 10.1038/nrn1909.
60. Kjaer S.L., Hougaard K.S., Tasker R.A., MacDonald D.S., Rosenberg R., Elfving B., et al. Influence of diurnal phase on startle response in adult rats exposed to dexamethasone in utero. Physiol Behav 2011, 102:444-452. 10.1016/j.physbeh.2010.12.015.
61. Zohar I., Weinstock M. Differential effect of prenatal stress on the expression of cortiocotrophin-releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats. J Neuroendocrinol 2011, 23:320-328. doi:10.1111/j.1365-2826.2011.02117.x; 10.1111/j.1365-2826.2011.02117.x.
62. Waford R.N., Lewine R. Is perseveration uniquely characteristic of schizophrenia?. Schizophr Res 2010, 118:128-133. 10.1016/j.schres.2010.01.031.
63. Arnsten A.F. Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 2009, 10:410-422. 10.1038/nrn2648.
64. Holscher C. Stress impairs performance in spatial water maze learning tasks. Behav Brain Res 1999, 100:225-235.
65. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev 2001, 36:60-90.
66. Hodges H. Maze procedures: the radial-arm and water maze compared. Cognitive Brain Res 1996, 3:167-181.
67. Bjorklund M., Sirvio J., Sallinen J., Scheinin M., Kobilka B.K., Riekkinen P. Alpha2C-adrenoceptor overexpression disrupts execution of spatial and non-spatial search patterns. Neuroscience 1999, 88:1187-1198.
68. Bjorklund M., Sirvio J., Riekkinen M., Sallinen J., Scheinin M., Riekkinen P. Overexpression of alpha2C-adrenoceptors impairs water maze navigation. Neuroscience 2000, 95:481-487.
69. Roof R.L., Stein D.G. Gender differences in Morris water maze performance depend on task parameters. Physiol Behav 1999, 68:81-86.
70. Faraji J., Metz G.A., Sutherland R.J. Characterization of spatial performance in male and female Long-Evans rats by means of the Morris water task and the ziggurat task. Brain Res Bull 2010, 81:164-172. 10.1016/j.brainresbull.2009.10.017.
71. Sutcliffe J.S., Marshall K.M., Neill J.C. Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 2007, 177:117-125. 10.1016/j.bbr.2006.10.029.
72. Bimonte H.A., Hyde L.A., Hoplight B.J., Denenberg V.H. In two species, females exhibit superior working memory and inferior reference memory on the water radial-arm maze. Physiol Behav 2000, 70:311-317.
73. Toufexis D. Region- and sex-specific modulation of anxiety behaviours in the rat. J Neuroendocrinol 2007, 19:461-473. 10.1111/j.1365-2826.2007.01552.x.