Neurosteroids infusion into the CA1 hippocampal region on exploration, anxiety-like behaviour and aversive learning

Behavioural Brain Research

Volumn 222, Issue 1, 2011, Pages 223-229

  Mòdol, Laura ^a   Darbra, Sònia ^a   Pallarès, Marc ^a  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

Author keywords

Allopregnanolone; Anxiety; Aversive learning; Exploration; Hippocampus; Pregnenolone sulphate

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; PRASTERONE SULFATE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; AVERSIVE BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; HIPPOCAMPAL CA1 REGION; HORMONE ACTION; LEARNING DISORDER; LEARNING TEST; MALE; MAZE TEST; MEMORY CONSOLIDATION; NEUROMODULATION; NEUROPATHOLOGY; NONHUMAN; PASSIVE AVOIDANCE; PATHOLOGICAL ANATOMY; PRIORITY JOURNAL; RAT;

EID: 79954604495     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.03.058     Document Type: Article

References (55)

1. Baulieu E.E., Fluxe K., Gustafsson J.A., Weterberg L. Steroid hormones in the brain: several mecahnism? In steroid hormone regulation of the brain 1981, Pergamon Press, Oxford, p. 3-14.
2. Dubrovsky B.O., Steroids neuroactive steroids and neurosteroids in psychopathology. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:169-192.
3. Mellon S.H. Neurosteroid regulation of central nervous system development. Pharmacol Ther 2007, 116:107-124.
4. Rupprecht R., di Michele F., Hermann B., Strohle A., Lancel M., Romeo E., et al. Neuroactive steroids: molecular mechanisms of action and implications for neuropsychopharmacology. Brain Res Brain Res Rev 2001, 37:59-67.
5. Mayo W., George O., Darbra S., Bouyer J.J., Vallée M., Darnaudéry M., et al. Individual differences in cognitive aging: implication of pregnenolone sulfate. Prog Neurobiol 2003, 71:43-48.
6. Frye C.A. Neurosteroids'effects and mechanisms for social, cognitive, emotional, and physical functions. Psychoneuroendocrinology 2009, 34(1):S143-161.
7. Rupprecht R. Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 2003, 28:139-168.
8. Rupprecht R., Holsboer F. Neuroactive steroids: mechanism of action and neuropsychopharmacological perpectives. Trends in Neurosci 1999, 22:410-416.
9. 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.
10. Kussius C.L., Kaur N., Popescu G.K. Pregnanolone sulfate promotes desensitization of activated NMDA receptors. J Neurosci 2009, 29:6819-6827.
11. Mtchedlishvili Z., Kapur J. A presynaptic action of neurosteroid pregnenolone sulfate on GABAergic synaptic transmission. Mol Pharmacol 2003, 64:857-864.
12. Frye C.A., Petralia S.M., Rhodes M.E. Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3α, 5α-THP. Pharmacol Biochem Behav 2000, 67:587-596.
13. Reddy D.S., Kulkarni S.K. Differential anxiolytic effects of neurosteroids in the mirrored chamber behavior test in mice. Brain Res 1997, 752:61-71.
14. Smith S.S. Withdrawal properties of neuroactive steroid: implicatons for GABAA receptor gene regulation in the brain and anxiety behaviour. Steroids 2002, 67:519-528.
15. Melchior C.L., Ritzmann R.F. Pregnenolone and pregnenolone suphate alone and with ethanol in mice on the plus-maze. Pharmacol Biochem Behav 1994, 43:813-819.
16. Akwa Y., Purdy R.H., Koob G.F., Britton K.T. The amygdala mediates the anxiolytic-like effect of the neurosteroid allopregnanolone in rat. Behav Brain Res 1999, 106:119-125.
17. Frye C.A., Walf A.A. Estrogen and/or progesterone administered systemically or to the amygdala can have anxiety-, fear-, and pain-reducing effects in ovarectomized rats. Behav Neurosci 2004, 118(2):306-313.
18. Frye C.A., Rhodes M.E. Infusions of 3α, 5α-THP to the VTA enahnce exploratory, anti-anxiety, social, and sexual behavior and increase levels of 3α,5α-THP in midbrain, hippocampus, diencephalon, and cortex of female rats. Behav Brain Res 2007, 187:88-99.
19. Frye C.A., Walf A.A. Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav 2002, 41:306-315.
20. Frye C.A., Walf A.A. Hippocampal 3α 5α-THP may alter behavior of pregnant and lactating rats. Pharmacol Biochem Behav 2004, 78:531-540.
21. Martin-Garcia E., Pallares M. Intrahippocampal nicotine and neurosteroids effects on the anxiety-like behaviour in voluntary and chronic alcohol-drinking rats. Behav Brain Res 2005, 164:117-127.
22. Bitran D., Dugan M., Renda P., Ellis R., Foley M. Anxiolytic effects of the neuroactive steroid pregnanolone (3 alpha-OH-5 beta-pregnan-20-one) after microinjection in the dorsal hippocampus and lateral septum. Brain Res 1999, 850:217-224.
23. Engin E., Treit D. The role of hippocampus in anxiety: intracerebral infusion studies. Behav Pharmacol 2007, 18:365-374.
24. Vallee M., Mayo W., Darnaudery M., Corpechot C., Young J., Koehl M., et al. Neurosteroids: deficient cognitive performance in aged rats depends on low pregnenolone sulfate levels in the hippocampus. PNAS 1997, 94(26):14865-14870.
25. Darnaudery M., Koehl M., Piazza P.V., Le Moal M., Mayo W. Pregnenolone sulfate increases hippocampal acetylcholine release and spatial recognition. Brain Res 2000, 852:173-179.
26. Johansson I.M., Birzniece V., Lindblad C., Olsson T., Backstrom T. Allopregnanolone inhibits learning in the Morris water maze. Brain Res 2002, 934:125-131.
27. 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.
28. 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. Proc Natl Acad Sci USA 1995, 92:10806-10810.
29. Martin-Garcia E., Pallares M. Apost-training intrahippocampal anxiogenic dose of neurosteroid pregnenolone sulphate impairs passive avoidance retention. Exp Brain Res 2008, 191:123-131.
30. Isaacson R.L., Varner J.A., Baars J., Wied D. The effects of pregnenolone sulfate ethylestrenol on retention of a passive avoidance task. Brain Res 1995, 678:79-84.
31. Vallee M., Shen W., Heinrichs S.C., Zorumski C.F., Covey D.F., Koob G.F., et al. Steroid structure and pharmacological properties determine the anti-amnesic effects of pregnenolone sulphate in the passive avoidance task in rats. Eur J Neurosci 2001, 14:2003-2010.
32. 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 Res 1993, 607:324-328.
33. 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. Alcohol Clin Exp Res 2002, 26:1747-1751.
34. 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 Res 2000, 858:371-379.
35. 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.
36. 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.
37. File S.E., Wardill A.G. The reliability of the hole-board apparatus. Psychopharmacology 1975, 44:47-51.
38. File S.E., Wardill A.G. Validity of head-dipping as a measure of exploration in a modified hole-board. Psychopharmacology 1975, 44:53-59.
39. 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. J Neurosci Methods 1985, 14:149-167.
40. Rodgers R.J., Dalvi A. Anxiety, defence and the elevated plus maze. Neurosc Biobehav Rev 1997, 21(6):801-810.
41. 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. Behav Brain Res 2008, 193:216-224.
42. Weiss S.M., Wadsworth G., Fletcher A., Dourish C.T. Utility of ethological analysis to overcome locomotor confounds in elevated plus maze. Neurosci Behav Rev 1998, 23:265-271.
43. Dawson G.R., Crawford S.P., Collinson N., Iversen S.D., Tricklebank M.D. Evidence that the anxiolytic-like affects of chlordiazepoxide on the elevated plus maze are counfounded by increases in locomotor activity. Psychopharmacology 1995, 118(3):316-323.
44. Takeda H., Tsuji M., Matsumiya T. Changes in head-dipping behavior in the hole-board test reflect the anxiogenic and/or anxiolytic state in mice. Eur J Pharmacol 1998, 350(1):21-29.
45. Vizi E.S., Kiss J.P. Neurochemistry and pharmacology of the major hippocampal transmitter system: synaptic and nonsynaptic interactions. Hippocampus 1998, 8:566-607.
46. Finn D.A., Roberts A.J., Long S., Tanchuck M., Phillips T.J. Neurosteroid consumption has anxiolytic effects in mice. Pharmacol Biochem Behav 2003, 76:451-462.
47. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., et al. Regional dissociations within the hippocampus--memory and anxiety. Neurosci Biobehav Rev 2004, 28:273-283.
48. Menard J., Treit D. The anxiolytic effects of intra-hippocampal midazolam are antagonized by intra-septal l-glutamate. Brain Res 2001, 888:163-166.
49. Bitran D., Foley M., Audette D., Leslie N., Frye C.A. Activation of peripheral mitochondrial benzodiazepine receptor in the hippocampus stimulates allopregnanolone synthesis and produces anxiolytic-like effects in the rat. Psychopharmacology 2000, 151:64-71.
50. Rhodes M.E., Frye C.A. Inhibiting progesterone metabolism in the hippocampus of rats in behavioral estrus decreases anxiolytic behaviors and enhances exploratory and antinociceptive behaviors. Cogn Affect Behav Neurosci 2000, 1:287-296.
51. Mathis C., Vogel B., Cagniard F., Criscuolo F., Ungerer A. The neurosteroid pregnenolone sulfate blocks deficits induced by a competitive NMDA antagonist in active avoidance and lever-press learning tasks in mice. Neuropharmacology 1996, 35(8):1057-1064.
52. Bowly M.R. Pregnenolone sulfate potentiation of NMDA receptor channels in hippocampal neurons. Mol Pharmacol 1993, 43:813-819.
53. Monnet F.P., Mahe V., Robel P., Baulieu E.E. Neurosteroids via sigma receptors modulate the (3H) norepinephrine release evoked by N-methil-d-aspartate in the rat hippocampus. Proc Natl Acad Sci USA 1995, 92:3774-3778.
54. Maurice T., Phan V.L., Urani A., Guillemain I. Differential involvement of the sigma 1 receptor in the anti-amnesic effect of neuroactive steroids, as demonstrated using an in vivo antisense strategy in the mouse. Br J Pharmacol 2001, 134:1731-1741.
55. Chida Y., Sudo N., Mori J., Kubo C. Social isolation stress impairs passive avoidance learning in senescence-accelerated mouse (SAM). Brain Res 2006, 1067:201-208.