Ethanol attenuates spatial memory deficits and increases mglu1a receptor expression in the hippocampus of rats exposed to prenatal stress

Alcoholism: Clinical and Experimental Research

Volumn 33, Issue 8, 2009, Pages 1346-1354

  Van Waes, Vincent ^a   Enache, Mihaela ^a   Zuena, Annarita ^a,b   Mairesse, Jérôme ^a,b   Nicoletti, Ferdinando ^b,c   Vinner, Elisabeth ^d   Lhermitte, Michel ^d   MacCari, Stefania ^a,b   Darnaudéry, Muriel ^a  

^a UNIV LILLE   (France)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c IRCCS NEUROMED   (Italy)

^d France Institut Pasteur de Lille   (France)

Author keywords

Alcohol; Glutamate; Lipid Peroxidation; Maternal Restraint Stress; Spatial Recognition

Indexed keywords

ALCOHOL; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 1A; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 5; UNCLASSIFIED DRUG;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; IMMOBILIZATION STRESS; MALE; MEMORY DISORDER; NONHUMAN; OXIDATIVE STRESS; PRENATAL EXPOSURE; PRENATAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPATIAL DISCRIMINATION; SPATIAL MEMORY; TASK PERFORMANCE;

ANIMALIA; RATTUS;

EID: 68149132856     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2009.00964.x     Document Type: Article

References (66)

1. Balschun D, Zuschratter W, Wetzel W (2006) Allosteric enhancement of metabotropic glutamate receptor 5 function promotes spatial memory. Neuroscience 142 : 691 702.
2. Beracochea D, Micheau J, Jaffard R (1992) Memory deficits following chronic alcohol consumption in mice: relationships with hippocampal and cortical cholinergic activities. Pharmacol Biochem Behav 42 : 749 753.
3. Cargiulo T (2007) Understanding the health impact of alcohol dependence. Am J Health Syst Pharm 64 : S5 11.
4. Champagne FA, Meaney MJ (2006) Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatry 59 : 1227 1235.
5. Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54 : 1025 1034.
6. Conrad CD, Galea LA, Kuroda Y, McEwen BS (1996) Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 110 : 1321 1334.
7. Darnaudery M, Louvart H, Defrance L, Leonhardt M, Morley-Fletcher S, Gruber SH, Galietta G, Mathe AA, Maccari S (2007) Impact of an intense stress on ethanol consumption in female rats characterized by their pre-stress preference: Modulation by prenatal stress. Brain Res 1131 : 181 186.
8. Darnaudery M, Maccari S (2008) Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57 : 571 585.
9. Darnaudery M, Perez-Martin M, Belizaire G, Maccari S, Garcia-Segura LM (2006) Insulin-like growth factor 1 reduces age-related disorders induced by prenatal stress in female rats. Neurobiol Aging 27 : 119 127.
10. Dellu F, Mayo W, Cherkaoui J, Le Moal M, Simon H (1992) A two-trial memory task with automated recording: study in young and aged rats. Brain Res 588 : 132 139.
11. Deminiere JM, Piazza PV, Guegan G, Abrous N, Maccari S, Le Moal M, Simon H (1992) Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res 586 : 135 139.
12. Dole VP, Ho A, Gentry RT (1985) Toward an analogue of alcoholism in mice: criteria for recognition of pharmacologically motivated drinking. Proc Natl Acad Sci USA 82 : 3469 3471.
13. Enache M, Van Waes V, Vinner E, Lhermitte M, Maccari S, Darnaudery M (2007) Impact of an acute exposure to ethanol on the oxidative stress status in the hippocampus of prenatal restraint stress adolescent male rats. Brain Res 1191C : 55 62.
14. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11 : 81 128.
15. Etchamendy N, Desmedt A, Cortes-Torrea C, Marighetto A, Jaffard R (2003) Hippocampal lesions and discrimination performance of mice in the radial maze: sparing or impairment depending on the representational demands of the task. Hippocampus 13 : 197 211.
16. Fadda F, Cocco S, Stancampiano R, Rossetti ZL (1999) Long-term voluntary ethanol consumption affects neither spatial nor passive avoidance learning, nor hippocampal acetylcholine release in alcohol-preferring rats. Behav Brain Res 103 : 71 76.
17. Fadda F, Rossetti ZL (1998) Chronic ethanol consumption: from neuroadaptation to neurodegeneration. Prog Neurobiol 56 : 385 431.
18. Fama R, Marsh L, Sullivan EV (2004) Dissociation of remote and anterograde memory impairment and neural correlates in alcoholic Korsakoff syndrome. J Int Neuropsychol Soc 10 : 427 441.
19. Farr SA, Scherrer JF, Banks WA, Flood JF, Morley JE (2005) Chronic ethanol consumption impairs learning and memory after cessation of ethanol. Alcohol Clin Exp Res 29 : 971 982.
20. Fujioka T, Fujioka A, Tan N, Chowdhury GM, Mouri H, Sakata Y, Nakamura S (2001) Mild prenatal stress enhances learning performance in the non-adopted rat offspring. Neuroscience 103 : 301 307.
21. Gal K, Bardos G (1994) The effect of chronic alcohol treatment on the radial maze performance of rats. Neuroreport 5 : 421 424.
22. Galindo R, Frausto S, Wolff C, Caldwell KK, Perrone-Bizzozero NI, Savage DD (2004) Prenatal ethanol exposure reduces mGluR5 receptor number and function in the dentate gyrus of adult offspring. Alcohol Clin Exp Res 28 : 1587 1597.
23. Genazzani AA, Casabona G, L'Episcopo MR, Condorelli DF, Dell'Albani P, Shinozaki H, Nicoletti F (1993) Characterization of metabotropic glutamate receptors negatively linked to adenylyl cyclase in brain slices. Brain Res 622 : 132 138.
24. Harwood HJ, Fountain D, Livermore G (1998) Economic costs of alcohol abuse and alcoholism. Recent Dev Alcohol 14 : 307 330.
25. Homewood J, Bond NW, MacKenzie A (1997) The effects of single and repeated episodes of thiamin deficiency on memory in alcohol-consuming rats. Alcohol 14 : 81 91.
26. Kalev-Zylinska ML, During MJ (2007) Paradoxical facilitatory effect of low-dose alcohol consumption on memory mediated by NMDA receptors. J Neurosci 27 : 10456 10467.
27. Kapoor A, Kostaki A, Janus C, Matthews SG (2009) The effects of prenatal stress on learning in adult offspring is dependent on the timing of the stressor. Behav Brain Res 197 : 144 149.
28. Kikkawa U, Ogita K, Ono Y, Asaoka Y, Shearman MS, Fujii T, Ase K, Sekiguchi K, Igarashi K, Nishizuka Y (1987) The common structure and activities of four subspecies of rat brain protein kinase C family. FEBS Lett 223 : 212 216.
29. Kippin TE, Szumlinski KK, Kapasova Z, Rezner B, See RE (2007) Prenatal Stress Enhances Responsiveness to Cocaine. Neuropsychopharmacology 33 : 769 782.
30. Koehl M, Bjijou Y, Le Moal M, Cador M (2000) Nicotine-induced locomotor activity is increased by preexposure of rats to prenatal stress. Brain Res 882 : 196 200.
31. Krazem A, Marighetto A, Higueret P, Jaffard R (2003a) Age-dependent effects of moderate chronic ethanol administration on different forms of memory expression in mice. Behav Brain Res 147 : 17 29.
32. Krazem A, Mons N, Higueret P, Jaffard R (2003b) Chronic ethanol consumption restores the age-related decrease in neurogranin mRNA level in the hippocampus of mice. Neurosci Lett 20 : 338.
33. Lemaire V, Koehl M, Le Moal M, Abrous DN (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97 : 11032 11037.
34. Li H, Li X, Jia N, Cai Q, Bai Z, Chen R, Song T, Zhu Z, Liu J (2008) NF-kappaB regulates prenatal stress-induced cognitive impairment in offspring rats. Behav Neurosci 122 : 331 339.
35. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ (2000) Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3 : 799 806.
36. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 17 : 5196 5205.
37. Lukoyanov NV, Madeira MD, Paula-Barbosa MM (1999) Behavioral and neuroanatomical consequences of chronic ethanol intake and withdrawal. Physiol Behav 66 : 337 346.
38. Maccari S, Morley-Fletcher S (2007) Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32 (Suppl. 1 S10 S15.
39. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M (1995) Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15 : 110 116.
40. Matthews DB, Morrow AL (2000) Effects of acute and chronic ethanol exposure on spatial cognitive processing and hippocampal function in the rat. Hippocampus 10 : 122 130.
41. Meunier J, Gue M, Recasens M, Maurice T (2004) Attenuation by a sigma1 (σ1) receptor agonist of the learning and memory deficits induced by a prenatal restraint stress in juvenile rats. Br J Pharmacol 142 : 689 700. (Pubitemid 38969664)
42. Morley-Fletcher S, Puopolo M, Gentili S, Gerra G, Macchia T, Laviola G (2004) Prenatal stress affects 3,4-methylenedioxymethamphetamine pharmacokinetics and drug-induced motor alterations in adolescent female rats. Eur J Pharmacol 489 : 89 92.
43. Mueller BR, Bale TL (2007) Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav 91 : 55 65.
44. Oscar-Berman M, Kirkley SM, Gansler DA, Couture A (2004) Comparisons of Korsakoff and non-Korsakoff alcoholics on neuropsychological tests of prefrontal brain functioning. Alcohol Clin Exp Res 28 : 667 675.
45. Pak JH, Huang FL, Li J, Balschun D, Reymann KG, Chiang C, Westphal H, Huang KP (2000) Involvement of neurogranin in the modulation of calcium/calmodulin-dependent protein kinase II, synaptic plasticity, and spatial learning: a study with knockout mice. Proc Natl Acad Sci USA 97 : 11232 11237.
46. Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34 : 1 26.
47. Reynaud M, Gaudin-Colombel AF, Le Pen C (2001) Two methods of estimating health costs linked to alcoholism in France (with a note on social costs). Alcohol Alcohol 36 : 89 95.
48. Riedel G, Casabona G, Platt B, Macphail EM, Nicoletti F (2000) Fear conditioning-induced time- and subregion-specific increase in expression of mGlu5 receptor protein in rat hippocampus. Neuropharmacology 39 : 1943 1951.
49. Riedel G, Wetzel W, Reymann KG (1996) Comparing the role of metabotropic glutamate receptors in long-term potentiation and in learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 20 : 761 789. (Pubitemid 26261909)
50. Robles N, Sabria J (2008) Effects of moderate chronic ethanol consumption on hippocampal nicotinic receptors and associative learning. Neurobiol Learn Mem 89 : 497 503.
51. Savage DD, Becher M, de la Torre AJ, Sutherland RJ (2002) Dose-dependent effects of prenatal ethanol exposure on synaptic plasticity and learning in mature offspring. Alcohol Clin Exp Res 26 : 1752 1758.
52. Schoepp DD, Jane DE, Monn JA (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38 : 1431 1476.
53. Simonyi A, Christian MR, Sun AY, Sun GY (2004) Chronic ethanol-induced subtype- and subregion-specific decrease in the mRNA expression of metabotropic glutamate receptors in rat hippocampus. Alcohol Clin Exp Res 28 : 1419 1423.
54. Smith JW, Seckl JR, Evans AT, Costall B, Smythe JW (2004) Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 29 : 227 244.
55. Son GH, Geum D, Chung S, Kim EJ, Jo JH, Kim CM, Lee KH, Kim H, Choi S, Kim HT, Lee CJ, Kim K (2006) Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci 26 : 3309 3318.
56. Steckler T, Oliveira AF, Van DC, Van CH, Mateus AM, Langlois X, Lesage AS, Prickaerts J (2005) Metabotropic glutamate receptor 1 blockade impairs acquisition and retention in a spatial Water maze task. Behav Brain Res 164 : 52 60.
57. Steigerwald ES, Miller MW (1997) Performance by adult rats in sensory-mediated radial arm maze tasks is not impaired and may be transiently enhanced by chronic exposure to ethanol. Alcohol Clin Exp Res 21 : 1553 1559.
58. Szuran TF, Pliska V, Pokorny J, Welzl H (2000) Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav 71 : 353 362.
59. Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, Aakalu VK, Lanahan AA, Sheng M, Worley PF (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23 : 583 592. (Pubitemid 29359928)
60. Vallee M, Maccari S, Dellu F, Simon H, Le Moal M, Mayo W (1999) Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur J Neurosci 11 : 2906 2916.
61. Van Waes V, Enache M, Dutriez I, Lesage J, Morley-Fletcher S, Vinner E, Lhermitte M, Vieau D, Maccari S, Darnaudery M (2006) Hypo-response of the hypothalamic-pituitary-adrenocortical axis after an ethanol challenge in prenatally stressed adolescent male rats. Eur J Neurosci 24 : 1193 1200.
62. Wu J, Song TB, Li YJ, He KS, Ge L, Wang LR (2007) Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats. Brain Res 1141 : 205 213.
63. Yaka R, Salomon S, Matzner H, Weinstock M (2007) Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behav Brain Res 179 : 126 132.
64. Yang J, Han H, Cao J, Li L, Xu L (2006a) Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 16 : 431 436.
65. Yang J, Li W, Liu X, Li Z, Li H, Yang G, Xu L, Li L (2006b) Enriched environment treatment counteracts enhanced addictive and depressive-like behavior induced by prenatal chronic stress. Brain Res 1125 : 132 137.
66. Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, Morley-Fletcher S, Chiodi V, Spagnoli LG, Gradini R, Catalani A, Nicoletti F, Maccari S (2008) Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE 3 : e2170.