Alterations in neonatal neurosteroids affect exploration during adolescence and prepulse inhibition in adulthood

Psychoneuroendocrinology

Volumn 35, Issue 4, 2010, Pages 525-535

  Darbra, Sònia ^a   Pallarès, Marc ^a  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

Author keywords

Allopregnanolone; Midazolam; Neurodevelopment; Neurosteroids; Novelty exploration; Prepulse inhibition

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; FINASTERIDE;

ADOLESCENCE; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; FEMALE; LOCOMOTION; MALE; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA; SENSORY GATING; STARTLE REFLEX; WEIGHT REDUCTION;

EID: 77950689114     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2009.08.020     Document Type: Article

References (64)

1. Adriani W., Granstrem O., Macri S., Izykenova G., Dambinova S., Laviola G. Behavioral and neurochemical vulnerability during adolescence in mice: studies with nicotine. Neuropsychopharmacology 2004, 29(5):869-878.
2. Adriani W., Laviola G. Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav. Pharmacol. 2004, 15(5-6):341-352.
3. Agís-Balboa R.C., Pinna G., Pibiri F., Kadriu B., Costa E., Guidotti A. Down-regulation of neurosteroid biosynthesis in corticolimbic circuits mediates social isolation-induced behavior in mice. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:18736-18741.
4. 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.
5. Azzolina B., Ellsworth K., Andersson S., Geissler W., Bull H.G., Harris G.S. Inhibition of rat α-reductases by finasteride: evidence for isozyme differences in the mechanism of inhibition. J. Steroid. Biochem. Mol. Biol. 1997, 61:55-64.
6. Baulieu E.E. Steroid hormones in the bra. Steroid Hormone Regulation of the Brain 1981, 3-14. Pergamon Press, Oxford. several mechanisms?, K. Fuxe, J.A. Gustafsson, L. Weterberg (Eds.).
7. Boissier J.R., Simon P. Automatisation du test de la planche à trous. Physiol. Behav. 1967, 2:447-448.
8. Braff D.L., Geyer M.A., Swerdlow N.R. Human studies of prepulse inhibition of startle: normal subjects patient groups and pharmacological studies. Psychopharmacology 2001, 156:234-258.
9. Brown G.R., Nemes C. The exploratory behaviour of rats in the hole-board apparatus: is head-dipping a valid measure of neophilia?. Behav. Process. 2008, 78(3):442-448.
10. Cooper E.J., Johnston G.A., Edwards F.A. Effects of a naturally occurring neurosteroid on GABAA IPSCs during development in rat hippocampal or cerebellar slices. J. Physiol. 1999, 521(Pt2):437-449.
11. Darbra S., Pallarès M. Neonatal allopregnanolone increases novelty-directed locomotion and disrupts behavioural responses to GABAA receptors modulators in adulthood. Int. J. Dev. Neurosci. 2009, 27(6):617-625.
12. Davis M., Walker D.L., Lee Y. Neurophysiology and neuropharmacology of startle and its affective modulation. Startle Modification. Implications for Neuroscience, Cognitive Science and Clinical Science 1999, 95-113. Cambridge University Press, Cambridge. M.E. Dawson, A.M. Schell, A.H. Bömehlt (Eds.).
13. Dubovicky M., Skultetyova I., Jezova D. Neonatal stress alters habituation of exploratory behavior in adult male but not female rats. Pharmacol. Biochem. Behav. 1999, 64:681-686.
14. Ellenbroek B.A., Cools A.R. Animal models for the negative symptoms of schizophrenia. Behav. Pharmacol. 2000, 11(3-4):223-233.
15. Ellenbroek B.A., Cools A.R. Early maternal deprivation and prepulse inhibition: the role of the postdeprivation environment. Pharmacol. Biochem. Behav. 2002, 73(1):177-184.
16. Ellenbroek B.A., van den Kroonenberg P.T., Cools A.R. Schizophr. Res. 1998, 30(3):251-260.
17. Engel S.R., Grant K.A. Neurosteroids and behavior. Int. Rev. Neurobiol. 2001, 46:321-348.
18. Escorihuela R.M., Fernández-Teruel A., Gil L., Aguilar R., Tobeña A., Driscoll P. Inbred Roman high- and low-avoidance rats: differences in anxiety, novelty-seeking, and shuttlebox behaviors. Physiol. Behav. 1999, 67:19-26. 1999.
19. File S.E., Wardill A.G. Validity of head-dipping as a measure of exploration in a modified hole-board. Psychopharmacologia 1975, 44(1):53-59.
20. Finn D.A., Ford M.M., Wiren K.M., Roselli C.E., Crabbe J.C. The role of pregnane neurosteroids in ethanol withdrawal: behavioral genetic approaches. Pharmacol. Ther. 2004, 101:91-112.
21. Follesa P., Biggio F., Caria S., Gorini G., Biggio G. Modulation of GABA (a) receptor gene expression by allopregnanolone and ethanol. Eur. J. Pharmacol. 2004, 500:413-425.
22. Frye C.A., Rhodes M.E., Petraglia S.M., Walf A.A., Sumida K., Edinger K.L. 3α-Hydroxy-5α-pregnan-20-one in the midbrain ventral tegmental area mediates social, sexual, and affective behaviors. Neuroscience 2006, 138:1007-1014.
23. Gizerian S.S., Morrow A.L., Lieberman J.A., Grobin A.C. Neonatal neurosteroid administration alters parvalbumin expression and neuron number in medial dorsal thalamus of adult rats. Brain Res. 2004, 1012:66-74.
24. Gizerian S.S., Moy S.S., Lieberman J.A., Grobin A.C. Neonatal neurosteroid administration results in development-specific alterations in prepulse inhibition and locomotor activity: neurosteroids alter prepulse inhibition and locomotor activity. Psychopharmacology 2006, 86:334-342.
25. Gogos A., van den Buuse M. The importance of baseline in identifying 8-OH-DPAT-induced effects on prepulse inhibition in rats. Br. J. Pharmacol. 2007, 150(6):750-757.
26. Grillon C., Ameli R., Foot M., Davis M. Fear-potentiated startle: relationship to the level of state/trait anxiety in healthy subjects. Biol. Psychiatry 1993, 33(8-9):566-574.
27. Grillon C., Ameli R., Woods S.W., Merikangas K., Davis M. Fear-potentiated startle in humans: effects of anticipatory anxiety on the acoustic blink reflex. Psychophysiology 1991, 28(5):588-595.
28. 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.
29. Grobin A.C., Heenan E.J., Lieberman J.A., Morrow A.L. Perinatal neurosteroid levels influence gabaergic interneuron localization in adult rat prefrontal cortex. J. Neurosci. 2003, 23:1832-1839.
30. Gruen R.J., Deutch A.Y., Roth R.H. Perinatal diazepam exposure: alterations in exploratory behavior and mesolimbic dopamine turnover. Pharmacol. Biochem. Behav. 1990, 36:169-175.
31. Gulinello M., Smith S.S. Anxiogenic effects of neurosteroid exposure: sex differences and altered GABAA receptor pharmacology in adult rats. J. Pharmacol. Exp. Ther. 2003, 305(2):541-548.
32. Iversen L. GABA pharmacology-what prospects for the future?. Biochem. Pharmacol. 2004, 68:1537-1540.
33. Kellogg C.K. Sex differences in long-term consequences of prenatal diazepam exposure: possible underlying mechanisms. Pharmacol. Biochem. Behav. 1999, 64:673-680.
34. Kilts C.D. The changing roles and targets for animals models of schizophrenia. Biol. Psychiatry 2001, 50:845-855.
35. Lambert J.J., Belelli D., Hill-Venning C., Peters J.A. Neurosteroids and GABAA receptor function. Trends Pharmacol. Sci. 1995, 16:295-303.
36. Laviola G., Macri S., Morley-Fletcher S., Adriani W. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 2003, 27:19-31.
37. Mameli M., Carta M., Partridge L.D., Valenzuela C.F. Neurosteroid-induced plasticity of immature synapses via retrograde modulation of presynaptic NMDA receptors. J. Neurosci. 2005, 25:2285-2294.
38. 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.
39. Martin-Garcia E., Pallares M. The intrahippocampal administration of the neurosteroid allopregnanolone blocks the audiogenic seizures induced by nicotine. Brain Res. 2005, 1062:144-150.
40. Martin-Garcia E., Darbra S., Pallares M. Neonatal finasteride induces anxiogenic-like profile and deteriorates passive avoidance in adulthood after intrahippocampal neurosteroid administration. Neuroscience 2008, 154:1497-1505.
41. Mellon S.H. Neurosteroid regulation of central nervous system development. Pharmacol. Ther. 2007, 116(1):107-124.
42. Mellon S.H., Griffin L.D. Neurosteroids: biochemistry and clinical significance. Trends Endocrinol. Metab. 2002, 13:35-43.
43. 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.
44. Mukai Y., Higashi T., Nagura Y., Shimada K. Studies on neurosteroids. XXV. Influence of a 5alpha-reductase inhibitor, finasteride, on rat brain neurosteroid levels and metabolism. Biol. Pharm. Bull. 2008, 31(9):1646-1650.
45. Muneoka K.T., Borella A., Whitaker-Azmitia P.M. Transient expression of s-100beta immunostaining in developing thalamus and somatosensory cortex of rat. Brain Res. Dev. Brain Res. 2003, 142:101-104.
46. Muneoka K., Takigawa T.M. A neuroactive steroid, pregnenolone, alters the striatal dopaminergic tone before and after puberty. Neuroendocrinology 2002, 75:288-295.
47. Pibiri F., Nelson M., Guidotti A., Pinna G. Decreased corticolimbic allopregnanolone expression during social isolation enhances contextual fear: a model relevant for posttraumatic stress disorder. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5567-5572.
48. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 2003, 463:3-33.
49. Purdy R.H., Morrow A.L., Moore P.H., Paul S.M. Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:4553-4557.
50. Reddy D.S. Physiological role of adrenal deoxycorticosterone-derived neuroactive steroids in stress-sensitive conditions. Neuroscience 2006, 138:911-920.
51. Reddy D.S., Kulkarni S.K. Sex and estrous cycle-dependent changes in neurosteroid and benzodiazepine effects on food consumption and plus-maze learning behaviors in rats. Pharmacol. Biochem. Behav. 1999, 62(1):53-60.
52. Riba J., Rodríguez-Fornells A., Urbano G., Morte A., Antonijoan R., Barbanoj M.J. Differential effects of alprazolam on the baseline and fear-potentiated startle reflex in humans: a dose-response study. Psychopharmacology (Berl.) 2001, 157(4):358-367.
53. 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.
54. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 2000, 24:417-463.
55. Swerdlow N.R., Martinez Z.A., Hanlon F.M., Platten A., Farid M., Auerbach P., Braff D.L., Geyer M.A. Toward understanding the biology of a complex phenotype: rat strain and substrain differences in the sensorimotor gating-disruptive effects of dopamine agonists. J. Neurosci. 2000, 20:4325-4336.
56. Swerdlow N.R., Geyer M.A., Braff D.L. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl.) 2001, 156(2-3):194-215.
57. Swerdlow N.R., Shoemaker J.M., Crain S., Goins J., Onozuka K., Auerbach P.P. Sensitivity to drug effects on prepulse inhibition in inbred and outbred rat strains. Pharmacol. Biochem. Behav. 2004, 77(2):291-302.
58. Swerdlow N.R., Light G.A., Cadenhead K.S., Sprock J., Hsieh M.H., Braff D.L. Startle gating deficits in a large cohort of patients with schizophrenia: relationship to medications, symptoms, neurocognition, and level of function. Arch. Gen. Psychiatry 2006, 63(12):1325-1335.
59. Thiel C.M., Muller C.P., Huston J.P., Schwarting R.K. High versus low reactivity to a novel environment: behavioural, pharmacological and neurochemical assessment. Neuroscience 1999, 93:243-251.
60. Vaglenova J., Birru S., Pandiella N.M., Breese C.R. An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav. Brain Res. 2004, 150:159-170.
61. Vallée 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 administration using negative chemical ionization gas chromatography/mass spectrometry. Anal. Biochem. 2000, 287(1):153-166.
62. van den Buuse M. Deficient prepulse inhibition of acoustic startle in Hooded-Wistar rats compared with Sprague-Dawley rats. Clin. Exp. Pharmacol. Physiol. 2003, 30(4):254-261.
63. Voikar V., Koks S., Vasar E., Rauvala H. Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol. Behav. 2001, 72:271-281.
64. Zimmerberg B., Rackow S.H., George-Friedman K.P. Sex-dependent behavioral effects of the neurosteroid allopregnanolone (3alpha, 5alpha-THP) in neonatal and adult rats after postnatal stress. Pharmacol. Biochem. Behav. 1999, 64(4):717-724.