Alteration of neonatal Allopregnanolone levels affects exploration, anxiety, aversive learning and adult behavioural response to intrahippocampal neurosteroids

Behavioural Brain Research

Volumn 241, Issue 1, 2013, Pages 96-104

  Mòdol, Laura ^a   Darbra, Sònia ^a   Vallèe, Monique ^b   Pallarès, Marc ^a  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

^b INSERM   (France)

Author keywords

Allopregnanolone; Anxiety like behaviour; Aversive learning; Development; Exploration; Finasteride; Hippocampus

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; FINASTERIDE; NEUROSTEROID; PREGNENOLONE SULFATE; SEPRANOLONE; TESTOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; AVERSIVE BEHAVIOR; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN LEVEL; CONTROLLED STUDY; EMOTIONALITY; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPAL CA1 REGION; HORMONE ACTION; HORMONE SYNTHESIS; LATENT PERIOD; LOCOMOTION; MALE; MAZE TEST; NEWBORN; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; RAT; SCREENING TEST; STIMULUS RESPONSE;

5-ALPHA REDUCTASE INHIBITORS; ANIMALS; ANXIETY; AVOIDANCE LEARNING; EXPLORATORY BEHAVIOR; FINASTERIDE; HIPPOCAMPUS; MALE; PREGNANOLONE; RATS; RATS, WISTAR;

EID: 84871844105     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.11.043     Document Type: Article

References (62)

1. Rupprecht R., Holsboer F. Neuroactive steroids: mechanism of action and neuropsychopharmacological perpectives. Trends in Neurosciences 1999, 22:410-416.
2. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 1986, 232:1004-1007.
3. Finn D.A., Roberts A.J., Long S., Tanchuck M., Phillips T.J. Neurosteroid consumption has anxiolytic effects in mice. Pharmacology Biochemistry and Behavior 2003, 76:451-462.
4. Reddy D.S., Kulkarni S.K. Differential anxiolytic effects of neurosteroids in the mirrored chamber behavior test in mice. Brain Research 1997, 752:61-71.
5. Akwa Y., Purdy R.H., Koob G.F., Britton K.T. The amygdala mediates the anxiolytic-like effect of the neurosteroid allopregnanolone in rat. Behavioural Brain Research 1999, 106:119-125.
6. Modol L., Darbra S., Pallares M. Neurosteroids infusion into CA1 hippocampal region non exploration, anxiety-like behaviour and aversive learning. Behavioural Brain Research 2011, 222(1):223-229.
7. Johansson I.M., Birzniece V., Lindblad C., Olsson T., Backstrom T. Allopregnanolone inhibits learning in the Morris water maze. Brain Research 2002, 934:125-131.
8. Mayo W., Dellu F., Robel P., Cherkaoui J., Le Moal M., Baulieu E.E., et al. Infusion of neurosteroids into the nucleus basalis magnocellularis affects cognitive processes in the rat. Brain Research 1993, 607:324-328.
9. Ladurelle N., Eychenne B., Denton D., Blair-West J., Schumacher M., Robel P., et al. Prolonged intracerebroventricular infusion of neurosteroids affects cognitive performances in the mouse. Brain Research 2000, 858:371-379.
10. Flood J.F., Morley J.E., Roberts E. Pregnenolone sulfate enhances post-training memory processes when injected in very low doses into limbic system structures: the amygdala is by far the most sensitive. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:10806-10810.
11. Williamson J., Mtchedlishvili Z., Kapur J. Characterization of the convulsant action of pregnenolone sulfate. Neuropharmacology 2004, 46:856-864.
12. Melchior C.L., Ritzmann R.F. Pregnenolone and pregnenolone suphate alone and with ethanol in mice on the pus-maze. Pharmacol 1993, 43:813-819.
13. Pallares M., Darnaudery M., Day J., Le Moal M., Mayo W. The neurosteroid pregnenolone sulfate infused into the nucleus basalis increases both acetylcholine release in the frontal cortex or amygdala and spatial memory. Neuroscience 1998, 87:551-558.
14. Martin-Garcia E., Pallares M. The neurosteroid pregnenolone sulfate neutralized the learning impairment induced by intrahippocampal nicotine in alcohol-drinking rats. Neuroscience 2005, 139(4):1109-1119.
15. Bowly M.R. Pregnenolone sulfate potentiation of NMDA receptor channels in hippocampal neurons. Molecular Pharmacology 1993, 43:813-819.
16. Darnaudery M., Koehl M., Piazza P.V., Le Moal M., Mayo W. Pregnenolone sulfate increases hippocampal acetylcholine release and spatial recognition. Brain Research 2000, 852:173-179.
17. Mameli M., Carta M., Partridge L.D., Valenzuela C.F. Neurosteroid induced plasticity of immature synapses via retrograde modulation of presynaptic NMDA receptors. Journal of Neuroscience 2005, 25:2285-2294.
18. Grobin A.C., Morrow A.L. 3Alpha-hydroxy-5alpha-pregnan-20-one levels and GABA(A) receptor-mediated 36Cl(-) flux across development in rat cerebral cortex. Brain Research Development 2001, 131(1-2):31-39.
19. Grobin A.C., Heenan E.J., Lieberman J.A., Morrow A.L. Perinatal neurosteroid levels influence GABAergic interneuron localization in adult rat prefrontal cortex. Journal of Neuroscience 2003, 23:1832-1839.
20. Griffin L.D., Gong W., Verot L., Mellon S.H. Niemann-pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nature Medicine 2004, 10:704-711.
21. Grobin A.C., Lieberman D.A., Morrow A.L. Perinatal flunitrazepam exposure causes persistent alteration of parvalbumin-immunoreactive interneuron localization in rat prefrontal cortex. Neuroscience Letters 2004, 359(1-2):9-12.
22. Grobin A.C., Gizerian S., Lieberman J.A., Morrow A.L. Perinatal allopregnanolone influences prefrontal cortex structure, connectivity and behavior in adult rats. Neuroscience 2006, 138:809-819.
23. Cooper E.J., Johnston G.A., Edwards F.A. Effects of a naturall occurring neurosteroid on GABAA IPSCs during development in rat hippocampal or cerebellar slices. Journal of Physiology 1999, 521(Pt 2):437-449.
24. Mellon S.H. Neurosteroid regulation of central nervous system development. Pharmacology & Therapeutics 2007, 116:107-124.
25. Mtchedlishvili Z., Sun C.S., Harrison M.B., Kapur J. Increased neurosteroid sensitivity of hippocampal GABAA receptors during postnatal development. Neuroscience 2003, 118:655-666.
26. Shirayama Y., Muneoka K.T., Iwata M., Ishida H., Hazama G., Kawahara R. Pregnenolone and dehydroepiandrosterone administration in neonatal rats alters the immunoreactivity of hippocampal synapsin I, neuropeptide Y and glial fibrillary acidic protein at post-puberty. Neuroscience 2005, 133:147-157.
27. Martin-Garcia E., Darbra S., Pallares M. Neonatal finasteride induces anxiogenic-like profile and deteriorates passive avoidance in adulthood after intrahippocampal neurosteoid administration. Neuroscience 2008, 154:1497-1505.
28. Darbra S., Pallares M. Alterations in neonatal neurosteroid affect exploration during adolescente and prepulse inhibition in the adulthood. Psychoneuroendocrinology 2010, 35(4):525-535.
29. Darbra S., Pallares M. Neonatal allopregnanolone increases novelty-directed locomotion and disrupts behavioural responses to GABA (A) receptor modulators in adulthood. International Journal of Developmental Neuroscience 2009, 27(6):617-625.
30. Darbra S., Pallares M. Interaction between early postnatal neurosteroid manipulations and adult infusion of neurosteroid into CA1 hippocampal region on the open field behaviour. Behavioural Brain Research 2011, 216(2):705-711.
31. Darbra S., Pallares M. Effects of early postnatal allopregnanolone administration on elevated plus maze anxiety scores in adult male Wistar rats. Neuropychobiology 2012, 65(1):20-27.
32. Vallee M., Rivera J.D., Koob G.F., Purdy R.H., Fitzgerald R.L. Quantification of neurosteroids in rat plasma and brain following swim stress and Allopregnanolone adminstration using negative chemicals ionization gas chromatography/mass spectrometry. Analytical Biochemistry 2000, 287:153-166.
33. Martin-Garcia E., Pallares M. Intrahippocampal nicotine and neurosteroids effects on the anxiety-like behaviour in voluntary and chronic alcohol-drinking rats. Behavioural Brain Research 2005, 164:117-127.
34. File S.E., Wardill A.G. The reliability of the hole-board apparatus. Psychopharmacology 1975, 44:47-51.
35. File S.E., Wardill A.G. Validity of head-dipping as a measure of exploration in modified hole-board. Psychopharmacology 1975, 44:53-59.
36. Pellow S., Chopin P., File S.E., Briley M. Validation of open closed arm entries in elevated plus-maze as a measur of anxiety in the rat. Journal of Neuroscience Methods 1985, 14:149-167.
37. Rodgers R.J., Dalvi A. Anxiety, defence and the elevated plus maze. Neuroscience & Biobehavioral Reviews 1997, 21(6):801-810.
38. Manhaes A.C., Guthierrez M.C.S., Filgueiras C.C., Abreu-Villaça Y. Anxiety-like behaviour during nicotine withdrawal predict subsequent nicotine compsumption in adolescent C57BL/6 mice. Behavioural Brain Research 2008, 193:216-224.
39. Turkmen S., Lundgren P., Birzniece V., Zingmark E., Backstrom T., Johansson I.M. 3b-20b-dihydroxy-5a-pregnane (UC1011) antagonism of the GABA potentiation and the learning impairment induced in rats by allopregnanolone. European Journal of Neuroscience 2004, 20:1604-1612.
40. Turkmen S., Lofgren M., Birzniece V., Backstrom T., Johansson I.M. Tolerance development to morris water maze test impairments induced by acute allopregnanolone. Neuroscience 2006, 139:651-659.
41. Kask K., Bäckström T., Nilsson L., Sundström-Poromaa I. Allopregnanolone impairs episodic memory in healthy women. Psychopharmacology 2008, 199:161-168.
42. Chin V.S., Van Skike C.E., Berry R.B., Kirk R.E., Diaz-Granados J., Matthews D.B. Effect of acute ethanol and acute allopregnanolone on spatial memory in adolescent and adult rats. Alcohol 2011, 45:473-483.
43. O'Dell L.E., Alomary A.A., Vallee M., Koob G.F., Fitzgerald R.L., Purdy R.H. Ethanol-induced increases in neuroactive steroids in the rat brain and plasma are absebt in adrenalectomized and gonadectomized rats. European Journal of Pharmacology 2004, 484(2-3):241-247.
44. Mellon S.H., Griffin L.D., Compagnone N.S. Biosynthesis and action of neurosteroids. Brain Research. Brain Research Reviews 2001, 37(1-3):3-12.
45. Compagnone N.A., Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Frontiers in Neuroendocrinology 2000, 21(1):1-56.
46. Azzolina B., Ellsworth K., Andersson S., Geissler W., Bull H.G., Harris G.S. Inhibition of rat alpha-reductases by finasteride: evidence for isozyme differences in the mechanism of inhibition. Journal of Steroid Biochemistry and Molecular Biology 1997, 61:55-64.
47. Poletti A., Coscarella A., Negri-Cesi P., Colciago A., Celotti F., Martini L. 5a-reductase isozymes in the central nervous system. Steroids 1998, 63:246-251.
48. Normington K., Russell D.W. Tissue distribution and kinetic characteristics of rat steroid 5a-reductase isozymes. Journal of Biological Chemistry 1992, 267:19548-19554.
49. Sierra A. Neurosteroids: the StAR protein in the brain. Journal of Neuroendocrinology 2004, 16(9):787-793.
50. Dubrovsky B.O. Steroids, neuroactive steroids and neurosteroids in psychopathology. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2005, 29:169-192.
51. Monnet F.P., Maurice T. The sigma1 protein as a target for the non-genomic effects of neuro(active)steroids: molecular, physiological, and behavioral aspects. Journal of Pharmaceutical Sciences 2006, 9(2):3-118.
52. Ben-Ari Y., Gaiarsa J.L., Tyzio R., Khazipov R.G.A.B.A. A pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiological Reviews 2007, 87:1215-1284.
53. Tyzio R., Minlebaev M., Rheims S., Ivanov A., Jorquera I., Holmes G.L., et al. Postnatal changes in somatic c-aminobutyric acid signalling in the rat hippocampus. European Journal of Neuroscience 2008, 27:2515-2528.
54. Stamatakis A., Pondiki S., Kitraki E., Diamantopoulou A., Panagiotaropoulos T., Raftogianni A., et al. Effect of neonatal handling on adult rat spatial learning and memory following acute stress. Stress 2008, 11(2):148-159.
55. Todeschin A.S., Winkelmann-Duarte E.C., Jacob M.H., Aranda B.C., Jacobs s Fernandes M.C., Ribeiro M.F., et al. Effect of neonatal handling on social memory: social interaction and number of oxytocin and vasopressin neurons in rats. Hormones and Behavior 2009, 56(1):93-100.
56. Matthews D.B., Morrow A.L., Tokunaga S., McDaniel J.R. Acute ethanol administration and acute allopregnanolone administration impair spatial memory in the Morris water task. Alcoholism, Clinical and Experimental Research 2002, 26:1747-1751.
57. Goodlett C.R., Jonhson T.B. Neonatal binge ethanol exposure using intubation: timing and dose effects on place learning. Neurotoxicology and Teratology 1997, 19(6):435-446.
58. Puglia M.P., Valenzuela C.F. AMPAR-mediated synaptic transmission in the CA1 hippocampal region of neonatal rats: unexpected resistance to repeated ethanol exposure. Alcohol 2010, 43:619-625.
59. Schummers J., Browning MD Evidence for a role for GABA(A) and NMDA receptors in ethanol inhibition of long-term potentiation. Brain Research Molecular Brian Research 2001, 94(1-2):9-14.
60. Van Doren M.J., Matthews D.B., Janis G.C., Grobin A.C., Devaud L.L., Morrow A.L. Neuroactive steroid 3alpha-hydroxy-5alpha- pregnan-20-one modulates electrophysiological and behavioral actions of ethanol. Journal of Neuroscience 2000, 20:1982-1989.
61. Silvers J.M., Tokunaga S., Berry R.B., White A.M., Matthews D.B. Impairments in spatial learning and memory: ethanol, allopregnanolone, and the hippocampus. Brain Research Reviews 2003, 43(3):275-284.
62. Silvers J.M., Tokunaga S., Mittleman G., O'Buckley T., Morrow L., 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 2006, 39:151-158.