Cognitive impairment and increased brain neurosteroids in adult rats perinatally exposed to low millimolar blood alcohol concentrations

Psychoneuroendocrinology

Volumn 32, Issue 8-10, 2007, Pages 931-942

  Barbaccia, Maria Luisa ^a   Scaccianoce, Sergio ^b   Del Bianco, Paola ^b   Campolongo, Patrizia ^b   Trezza, Viviana ^b   Tattoli, Maria ^c   Cuomo, Vincenzo ^b   Steardo, Luca ^b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF BARI   (Italy)

Author keywords

3 hydroxy 5 pregnan 20 one (allopregnanolone, 3 ,5 THP); Developmental alcohol; Elevated plus maze; Inhibitory avoidance; Progesterone; Social recognition memory

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; ALCOHOL; NEUROSTEROID; PREGNENOLONE; PROGESTERONE; SUCROSE;

ALCOHOL BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN CORTEX; BRAIN DEVELOPMENT; COGNITIVE DEFECT; CONTROLLED STUDY; EMOTION; FEMALE; FETAL ALCOHOL SYNDROME; FETUS; GENE AMPLIFICATION; MAZE TEST; MEMORY CONSOLIDATION; NEUROTRANSMISSION; NEWBORN; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; RAT; SKILL; SOCIAL BEHAVIOR; SOCIAL DISCRIMINATION; STEROID RELEASE; TASK PERFORMANCE;

ALCOHOL DRINKING; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; COGNITION DISORDERS; ETHANOL; FEMALE; LACTATION; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; REPRODUCTION; STEROIDS;

EID: 36048963648     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2007.06.013     Document Type: Article

References (96)

1. Agis-Balboa R.C., Pinna G., Zhubi A., Maloku E., Veldic M., Costa E., and Guidotti A. Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proc. Nat. Acad. Sci. USA 103 (2006) 14602-14607
2. A receptor-gated chloride ions channel in adult rat offspring. J. Pharmacol. Exp. Ther. 284 (1998) 250-257
3. Anglade F., Chapoutier G., Dodd R.H., and Baudoin C. Olfactory memory in rats, cholinergic agents and benzodiazepine receptor ligands. J. Physiol. (Paris) 93 (1999) 225-232
4. Auger C.J., and Vanzo R.J. Progesterone treatment of adult male rats suppresses arginine vasopressin expression in the adult bed nucleus of the stria terminalis and the centromedial amygdala. J. Neuroendocrinol. 18 (2006) 187-194
5. Barbaccia M.L. Neurosteroidogenesis: relevance to neurosteroid actions in brain and modulation by psychotropic drugs. Crit. Rev. Neurobiol. 16 (2004) 67-74
6. Barbaccia M.L., Affricano D., Trabucchi M., Purdy R.H., Colombo G., Agabio R., and Gessa G.L. Ethanol markedly increases "GABAergic" neurosteroids in alcohol preferring rats. Eur. J. Pharmacol. 384 (1999) R1-R2
7. A receptor function after acute stress. Neuroendocrinology 63 (1996) 166-172
8. A receptor active neurosteroids and the sedative/hypnotic action of γ-hydroxybutyric acid (GHB): a study in GHB-S(sensitive) and GHB-R(resistant) rat lines. Neuropharmacology 49 (2005) 48-58
9. Battaini F., Pascale A., Ancona D.M.R., Cagiano R., Cuomo V., and Govoni S. Moderate alcohol intake: behavioral and neurochemical correlates in rats. Nutr. Neurosci. 1 (1998) 151-159
10. Baulieu E.-E. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 23 (1998) 963-987
11. A receptor. Nat. Rev. Neurosci. 6 (2005) 565-575
12. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3 (2002) 728-739
13. Bitran D., Dugan M., Renda P., Ellis R., and Foley M. Anxiolytic effects of the neuroactive steroid pregnanolone (3α-OH-5β-pregnan-20-one) after microinjection in the dorsal hippocampus and lateral septum. Brain Res. 850 (1999) 217-224
14. Bitran D., Foley M., Audette D., Leslie N., and Frye C.A. Activation of peripheral mitochondrial benzodiazepine receptors in the hippocampus stimulates allopregnanolone synthesis and produces anxiolytic-like effects in the rat. Psychopharmacology 151 (2000) 64-71
15. Breese G.R., Criswell H.E., Carta M., Dodson P.D., Hanchar H.J., Khisti R.T., Mameli M., Ming Z., Morrow A.L., Olsen R.W., Otis T.S., Parsons L.H., Penland S.N., Roberto M., Siggins G.R., Valenzuela C.F., and Wallner M. Basis of Gabamimetic profile of ethanol. Alcohol. Clin. Exp. Res. 30 (2006) 731-744
16. Brown R.T., Coles C.D., Smith I.E., Platzman K.A., Silverstein J., Erikson S., and Falek A. Effects of prenatal alcohol exposure at school age. II. Attention and behaviour. Neurotoxicol. Teratol. 13 (1991) 369-376
17. Caetano R., Ramisetty-Mikler S., Floyd L.R., and McGrath C. The epidemiology of drinking among women of child-bearing age. Alcohol. Clin. Exp. Res. 30 (2006) 1023-1030
18. Cagetti E., Pinna G., Guidotti A., Baicy K., and Olsen R.W. Chronic intermittent ethanol (CIE) administration in rats decreases level of neurosteroids in hippocampus, accompanied by altered behavioral responses to neurosteroids and memory function. Neuropharmacology 46 (2004) 570-579
19. Cagiano R., Tattoli M., Persichella M., Mazzoccoli M., Govoni S., and Cuomo V. Effects of chronic low-dose ethanol intake on sexual behavior in rats. Alcohol 16 (1998) 135-138
20. Cagiano R., Cassano T., Coluccia A., Gaetani S., Giustino A., Steardo L., Tattoli M., Trabace L., and Cuomo V. Genetic factors involved in the effects of developmental low-level alcohol induced behavioral alterations in rats. Neuropsychopharmacology 26 (2002) 191-203
21. Caldeira J.C., Wu Y., Mameli M., Purdy R.H., Li P.-K., Akwa Y., Savage D.D., Engen J.R., and Valenzuela C.F. Fetal alcohol exposure alters neurosteroid levels in the developing rat brain. J. Neurochem. 90 (2004) 1530-1539
22. Chambers C.D., Hughes S., Meltzer S.B., Wahlgren D., Kassem N., Larson S., Riley E.P., and Hovell M.F. Alcohol consumption among low-income pregnant latinas. Alcohol. Clin. Exper. Res. 29 (2005) 2022-2028
23. Cheney D.L., Uzunov D.P., and Guidotti A. Pregnenolone sulfate antagonizes dizocilpine amnesia: role for allopregnanolone. Neuroreport 6 (1995) 1697-1700
24. Colvin L., Payne J., Parsons D., Kurinczuk J.J., and Bower C. Alcohol consumption during pregnancy in nonindigenous west Australian women. Alcohol. Clin. Exp. Res. 31 (2007) 276-284
25. Compagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinology 21 (2000) 1-56
26. Concas A., Mostallino M.C., Porcu P., Follesa P., Barbaccia M.L., Trabucchi M., Purdy R.H., Grisenti P., and Biggio G. Role of brain allopregnanolone in the plasticity of gamma-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc. Nat. Acad. Sci. USA 95 (1998) 13284-13289
27. Constantinidis C., Williams G.V., and Goldman-Rakic P.S. A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat. Neurosci. 5 (2002) 175-180
28. Costa E., and Guidotti A. Benzodiazepiness on trial: a research strategy for their rehabilitation. Trends Pharmacol. Sci. 17 (1996) 192-200
29. Costa L.G., Steardo L., and Cuomo V. Structural effects and neurofunctional sequelae of developmental exposure to psychotherapeutic drugs: experimental and clinical aspects. Pharmacol. Rev. 56 (2004) 103-147
30. Crews F.T., Morrow A.L., Criswell H., and Breese G. Effects of ethanol on ion channels. Int. Rev. Neurobiol. 39 (1996) 283-367
31. Dantzer R., Bluthe R.M., Koob G.F., and Le Moal M. Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology (Berlin) 91 (1987) 363-368
32. Dantzer R., Koob G.F., Bluthe R.M., and Le Moal. M. Septal vasopressin modulates social memory in male rats. Brain Res. 457 (1988) 143-147
33. Eckardt M.J., File S.E., Gessa G.L., Grant K.A., Guerri C., Hoffman P.L., Kalant H., Koob G.F., and Tabakoff B. Effects of moderate alcohol consumption on the central nervous system. Alcohol. Clin. Exp. Res. 22 (1998) 998-1040
34. Engelmann M., Wotjak C.T., and Landgraf R. Social discrimination procedure: an alternative method to investigate juvenile recognition abilities in rats. Physiol. Behav. 58 (1995) 315-321
35. Epperson C.N., deWit H., and Krystal J.H. Advances in the translational neuroscience of neurosteroids. Psychopharmacology 186 (2006) 265-266
36. Famy C., Streissguth A.P., and Unis A.S. Mental illness in adults with fetal alcohol syndrome or fetal alcohol effects. Am. J. Psychiatry 155 (1998) 552-554
37. Ferguson J.N., Young L.J., and Insel T.R. The neuroendocrine basis of social recognition. Front. Neuroendocrinol. 23 (2002) 200-224
38. Ford M.M., Nickel J.D., and Finn D.A. Treatment and withdrawal from finasteride alter ethanol intake patterns in male C57BL/6J mice: potential role of endogenous neurosteroids?. Alcohol 37 (2005) 23-33
39. Freeman F.M., and Young I.G. The mitochondrial benzodiazepine receptor and avoidance learning in the day-old chick. Pharmacol. Biochem. Behav. 67 (2000) 355-362
40. Frye C.A., Edinger K.L., Seliga A.M., and Wawrzycki J.M. 5Alpha-reduced androgens may have actions in the hippocampus to enhance cognitive performance of male rats. Psychoneuroendocrinology 29 (2004) 1019-1027
41. Frye C.A., Rhodes M.E., Raol Y.S., and Brooks-Kayal A.R. Early postnatal stimulation alters pregnane neurosteroids in the hippocampus. Psychopharmacology 186 (2006) 343-350
42. Galindo R., Zamudio P.A., and Valenzuela C.F. Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J. Neurochem. 94 (2005) 1500-1511
43. George O., Vallée M., Le Moal M., and Mayo W. Neurosteroids and cholinergic systems: implications for sleep and cognitive processes and potential role of age-related changes. Psychopharmacology 186 (2006) 402-413
44. Govoni S., Trabucchi M., Cagiano R., and Cuomo V. Alcohol and the brain: setting the benefit/risk balance. Alcohol 11 (1994) 241-246
45. Grazzini E., Guillon G., Mouillac B., and Zingg H.H. Inhibition of oxytocin receptor function by direct binding of progesterone. Nature 392 (1998) 509-512
46. Grobin A.C., Gizerian S., Lieberman J.A., and Morrow A.L. Perinatal allopregnanolone influences prefrontal cortex structure, connectivity and behavior in adult rats. Neuroscience 138 (2006) 809-819
47. Hannigan J.H. What research with animals is telling us about alcohol-related neurodevelopmental disorders. Pharmacol. Biochem. Behav. 55 (1996) 489-499
48. Hirani K., Sharma A.N., Jain N.S., Ugale R.R., and Chopde C.T. Evaluation of GABAergic neuroactive steroid 3α-hydroxy-5α-pregnane-20-one as a neurobiological substrate for the anti-anxiety effect of ethanol in rats. Psychopharmacology 180 (2005) 267-278
49. A receptors through two discrete transmembrane sites. Nature 444 (2006) 486-489
50. 4 isomerase in the rat brain. Endocrinology 144 (2003) 2902-2911
51. Ikonomidou C., Bittigau P., Ishimaru M.J., Wozniak D.F., Koch C., Genz K., Price M.T., Stefovska V., Horster F., Tenkova T., Dikranian K., and Olney JW. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 287 (2000) 1056-1060
52. Janis G.C., Devaud L.L., Mitsuyama H., and Morrow A.L. Effects of chronic ethanol consumption and withdrawal on the neuroactive steroid 3alpha-hydroxy-5alpha-pregnan-20-one in male and female rats. Alcohol. Clin. Exp. Res. 22 (1998) 2055-2061
53. Jung-Testas I., Hu Z.Y., Baulieu E.-E., and Robel P. Neurosteroids: biosynthesis of pregnenolone and progesterone in primary cultures of rat glial cells. Endocrinology 125 (1989) 2083-2091
54. Kelly S.J., and Tran T.D. Alcohol exposure during development alters social recognition and social communication in rats. Neurotoxicol. Teratol. 19 (1997) 383-389
55. Kelly S.J., Day N., and Streissguth A.P. Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicol. Teratol. 22 (2000) 143-149
56. Khisti R.T., Van Doren M.J., O'Buckley T., and Morrow A.L. Neuroactive steroid 3alpha-hydroxy-5alpha-pregnan-20-one modulates ethanol-induced loss of righting reflex in rats. Brain Res. 980 (2003) 255-263
57. Kimoto T., Tsurugizawa T., Ohta Y., Makino J., Tamura H., Hoyo Y., Takata N., and Kawato S. Neurosteroid synthesis by cytochrome p450-containing systems localized in the rat brain hippocampal neurons: N-methyl-d-aspartate and calcium-dependent synthesis. Endocrinology 142 (2001) 3578-3589
58. Kohchi C., Ukena K., and Tsutsui K. Age- and region-specific expression of the messenger RNAs encoding for steroidogenic enzymes P450scc, P450c17 and 3beta-HSD in the postnatal rat brain. Brain Res. 801 (1998) 233-238
59. Kristjanson A.F., Wilsnack S.C., Zvartau E., Tsoy M., and Novikov B. Alcohol use in pregnant and nonpregnant Russian women. Alcohol. Clin. Exp. Res. 31 (2007) 299-307
60. Ladurelle N., Eychenne B., Denton D., Blair-West J., Schumacher M., Robel P., and Baulieu E.-E. Prolonged intracerebroventricular infusion of neurosteroids affects cognitive performance in the mouse. Brain Res. 858 (2000) 371-379
61. Lauber M.E., and Lichtensteiger W. Ontogeny of 5α-reducatse (Type 1) messenger ribonucleic acid expression in rat brain: early presence in germinal zones. Endocrinology 137 (1996) 2718-2730
62. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-276
63. Maier S.E., Miller J.A., Blackwell J.M., and West J.R. Fetal alcohol exposure and temporal vulnerability: regional differences in cell loss as a function of the timing of binge-like alcohol exposure during brain development. Alcohol. Clin. Exp. Res. 23 (1999) 726-734
64. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 (1986) 1004-1007
65. Mameli M., and Valenzuela F.C. Alcohol increases efficacy of immature synapses in a neurosteroid-dependent manner. Eur. J. Neurosci. 23 (2006) 835-839
66. Matsumoto K., Uzunova V., Pinna G., Taki K., Uzunov D.P., Watanabe H., Mienville J.-M., Guidotti A., and Costa E. Permissive role of brain allopregnanolone content in the regulation of pentobarbital-induced righting reflex loss. Neuropharmacology 38 (1999) 955-963
67. Mattson S.N., and Riley E.P. A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin. Exp. Res. 22 (1998) 279-294
68. Mereu G., Fa M., Ferraro L., Cagiano R., Antonelli T., Tattoli M., Giglieri V., Manganelli S., Gessa G.L., and Cuomo V. Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfunction in hippocampal long-term potentiation and glutamate release. Proc. Nat. Acad. Sci. USA 100 (2003) 4915-4920
69. Morrow A.L., VanDoren M.J., Penland S.N., and Matthews D.B. The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res. Brain Res. Rev. 37 (2001) 98-109
70. Patchev V.K., Hassan A.H.S., Holsboer F., and Almeida O.F.X. The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15 (1996) 533-540
71. Paulsen O., and Moser E.I. A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci. 21 (1998) 273-278
72. Pellow S., Chopin P., File S.E., and Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Method 14 (1985) 149-167
73. Penn A.A., and Schatz C.J. Brain waves and brain wiring: the role of endogenous and sensory-driven neural activity in development. Pediatr. Res. 45 (1999) 447-458
74. Petrulis A., Alvarez P., and Eichenbaum H. Neural correlates of social odor recognition and the representation of individual distinctive social odors within entorhinal cortex and ventral subiculum. Neuroscience 130 (2005) 259-274
75. Pinna G., Costa E., and Guidotti A. Fluoxetine and norfluoxetine stereospecifically and selectively increase brain neurosteroid content at doses that are inactive on 5-HT reuptake. Psychopharmacology 186 (2006) 362-372
76. A receptor agonist muscimol. Neuropharmacology 39 (2000) 440-448
77. Popik P., and van Ree J.M. Neurohypophyseal peptides and social recognition in rats. Prog. Brain Res. 119 (1998) 415-436
78. Popik P., Vetulani J., Bisaga A., and van Ree J.M. Recognition cue in the rat's social memory paradigm. J. Basic Clin. Physiol. Pharmacol. 2 (1991) 315-327
79. A receptor function. Neuropharmacology 44 (2003) 49-55
80. Purdy R.H., Morrow A.L., Blinn J.R., and Paul S.M. Synthesis, metabolism and pharmacological activity of 3α-hydroxysteroids which potentiate GABA-receptor-mediated chloride ion uptake in cerebrocortical synaptoneurosomes. J. Med. Chem. 33 (1990) 1572-1581
81. Romeo E., Cheney D.L., Zivkovich I., Costa E., and Guidotti A. Mitochondrial diazepam-binding inhibitor receptor complex agonists antagonize dizocilpine amnesia: putative role for allopregnanolone. J. Pharmacol. Exp. Ther. 270 (1994) 89-96
82. Roscetti G., Del Carmine R., Trabucchi M., Massotti M., Purdy R..H., and Barbaccia M.L. Modulation of neurosteroid synthesis/acculmulation by l-ascorbic acid in rat brain tissue: inhibition by selected serotonin antagonists. J. Neurochem. 71 (1998) 1108-1117
83. Rupprecht R., and Holsboer F. Neuroactive steroids: mechanisms of action and neuropshychopharmacological perspectives. Trends Neurosci. 22 (1999) 410-416
84. A receptor activity in rat hippocampus. J. Neurosci. 24 (2004) 6521-6530
85. A receptor function in rat brain. J. Neurochem. 75 (2000) 732-740
86. Shaywitz S.E., Cohen D.J., and Shaywitz B.A. Behavior and learning difficulties in children of normal intelligence born to alcoholic mothers. J. Pediatrics 96 (1980) 978-982
87. Silvers J., Tokunaga S., Mittleman G., O'Buckley T., Morrow A.L., and Matthews D.B. Chronic intermittent ethanol exposure during adolescence reduces the effect of ethanol challenge on hippocampal allopregnanolone levels and Morris water maze task performance. Alcohol 39 (2006) 151-158
88. Sood B., Delaney-Black V., Covington C., Nordstrom-Klee B., Ager J., Templin T., Janisse J., Martier S., and Sokol R.J. Prenatal alcohol exposure and childhood behavior at age 6 to 7 years: I. Dose-response effect. Pediatrics 108 (2001) 34-42
89. Stackman, R.W., McCarthy, K.A., Yoneyama, N., Tull, L.E., Finn, D.A., 2005. Allopregnanolone impairs hippocampal-dependent object recognition memory in C57BL/6J mice. Program No. 998.5 2005 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, DC, 2005 (Online).
90. Strous R.D., Maayan R., and Weizman A. The relevance of neurosteroids to clinical psychiatry: from the laboratory to the bedside. Eur. Neuropsychopharmacol. 16 (2006) 155-169
91. Tattoli M., Cagiano R., Gaetani S., Ghiglieri V., Giustino A., Mereu G., Trabace L., and Cuomo V. Neurofunctional effects of developmental alcohol exposure in alcohol-preferring and alcohol-nonpreferring rats. Neuropsychopharmacology 24 (2001) 691-705
92. Tsutsui K., Ukena K., Usui M., Sakamoto H., and Takase M. Novel brain function: biosynthesis and action of neurosteroids in neurons. Neurosci. Res. 36 (2000) 261-273
93. Van Doren M.J., Matthews D.B., Janis G., Grobin A.C., Devaud L.L., and Morrow A.L. Neuroactive steroid 3alpha-hydroxy-5α-pregnan-20-one modulates electrophysiological and behavioral actions of ethanol. J. Neurosci. 20 (2000) 1982-1989
94. Winocur G. The hippocampus and thalamus: their roles in short- and long-term memory and the effects of interference. Behav. Brain Res. 16 (1985) 135-152
95. Zimmerberg B., and Brown R.C. Prenatal experience and postnatal stress modulate the adult neurosteroid and catecholaminergic stress response. Int. J. Dev. Neurosci. 16 (1998) 217-228
96. Zimmerberg B., Brunelli S., Fluty A.J., and Frye C.A. Differences in affective behaviors and hippocampal allopregnanolone levels in adult rats of lines selectively bred for infantile vocalizations. Behav. Brain Res. 159 (2005) 301-311