Role of gonadal hormones in anxiety and fear memory formation and inhibition in male mice

Physiology and Behavior

Volumn 105, Issue 5, 2012, Pages 1168-1174

  McDermott, Carmel M ^a   Liu, Dana ^a   Schrader, Laura A ^a,b  

^a Tulane University   (United States)

^b TULANE UNIVERSITY   (United States)

Author keywords

Castration; Elevated Plus Maze; Extinction; Fear conditioning; Hippocampus; Open Field Assay; Puberty

Indexed keywords

SEX HORMONE; TESTOSTERONE;

AGING; ANXIETY; ARTICLE; BEHAVIOR; CASTRATION; CONTROLLED STUDY; FEAR; INHIBITION (PSYCHOLOGY); MALE; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PUBERTY; REINFORCEMENT;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; ASSOCIATION LEARNING; BEHAVIOR, ANIMAL; CASTRATION; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; INHIBITION (PSYCHOLOGY); MALE; MEMORY; MICE; MICE, 129 STRAIN; SEX FACTORS; SEXUAL MATURATION; TESTOSTERONE;

EID: 84862823354     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.12.016     Document Type: Article

References (54)

1. Pigott T.A. Anxiety disorders in women. Psychiatr Clin North Am 2003, 26(3):621-672. vi-vii.
2. Kaminetsky J.C. Benefits of a new testosterone gel formulation for hypogonadal men. Clin Cornerstone 2005, 7(Suppl 4):S8-S12.
3. Veras A.B., Nardi A.E. The complex relationship between hypogonadism and major depression in a young male. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34(2):421-422.
4. Cooper M.A., Ritchie E.C. Testosterone replacement therapy for anxiety. Am J Psychiatry 2000, 157(11):1884.
5. Barrett-Connor E., Von Muhlen D.G., Kritz-Silverstein D. Bioavailable testosterone and depressed mood in older men: the Rancho Bernardo Study. J Clin Endocrinol Metab 1999, 84(2):573-577.
6. Tolin D.F., Foa E.B. Sex differences in trauma and posttraumatic stress disorder: a quantitative review of 25 years of research. Psychol Bull 2006, 132(6):959-992.
7. McEwen B.S. Gonadal steroids and brain development. Biol Reprod 1980, 22(1):43-48.
8. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24(4):417-463.
9. Spear L.P. Adolescence and the trajectory of alcohol use: introduction to part VI. Ann N Y Acad Sci 2004, 1021:202-205.
10. Granger D.A., et al. Salivary testosterone diurnal variation and psychopathology in adolescent males and females: individual differences and developmental effects. Dev Psychopathol 2003, 15(2):431-449.
11. Schulz K.M., et al. Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syrian hamster. Horm Behav 2004, 45(4):242-249.
12. Schulz K.M., Sisk C.L. Pubertal hormones, the adolescent brain, and the maturation of social behaviors: Lessons from the Syrian hamster. Mol Cell Endocrinol 2006, 254-255:120-126.
13. Schulz K.M., et al. Testicular hormone exposure during adolescence organizes flank-marking behavior and vasopressin receptor binding in the lateral septum. Horm Behav 2006, 50(3):477-483.
14. Zehr J.L., et al. Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. J Neurobiol 2006, 66(6):578-590.
15. Zehr J.L., et al. Adolescent development of neuron structure in dentate gyrus granule cells of male Syrian hamsters. Dev Neurobiol 2008, 68(14):1517-1526.
16. Ho A., et al. The pubertal-related decline in cellular proliferation and neurogenesis in the dentate gyrus of male rats is independent of the pubertal rise in gonadal hormones. Dev Neurobiol 2011, 10.1002/dneu.20987.
17. Edinger K.L., Lee B., Frye C.A. Mnemonic effects of testosterone and its 5alpha-reduced metabolites in the conditioned fear and inhibitory avoidance tasks. Pharmacol Biochem Behav 2004, 78(3):559-568.
18. Anagnostaras S.G., et al. Testicular hormones do not regulate sexually dimorphic Pavlovian fear conditioning or perforant-path long-term potentiation in adult male rats. Behav Brain Res 1998, 92(1):1-9.
19. Frye C.A., Edinger K., Sumida K. Androgen administration to aged male mice increases anti-anxiety behavior and enhances cognitive performance. Neuropsychopharmacology 2008, 33(5):1049-1061.
20. Agis-Balboa R.C., et al. Enhanced fear responses in mice treated with anabolic androgenic steroids. Neuroreport 2009, 20(6):617-621.
21. Myers K.M., Davis M. Mechanisms of fear extinction. Mol Psychiatry 2007, 12(2):120-150.
22. McCallum J., Kim J.H., Richardson R. Impaired extinction retention in adolescent rats: effects of D-cycloserine. Neuropsychopharmacology 2010, 35(10):2134-2142.
23. Kim J.H., Richardson R. Extinction in preweanling rats does not involve NMDA receptors. Neurobiol Learn Mem 2010, 94(2):176-182.
24. Hefner K., Holmes A. Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav Brain Res 2007, 176(2):210-215.
25. Wainman P., Shipounoff G.C. The effects of castration and testosterone propionate on the striated perinal musculature in the rat. Endocrinology 1941, 29:975-978.
26. Laroche J., et al. Reduced behavioral response to gonadal hormones in mice shipped during the peripubertal/adolescent period. Endocrinology 2009, 150(5):2351-2358.
27. Zuloaga D.G., Jordan C.L., Breedlove S.M. The Organizational Role of Testicular Hormones and the Androgen Receptor in Anxiety-Related Behaviors and Sensorimotor Gating in Rats. Endocrinology 2011, 152(4):1572-1581.
28. Benice T.S., Raber J. Dihydrotestosterone modulates spatial working-memory performance in male mice. J Neurochem 2009, 110(3):902-911.
29. Frye C.A., Seliga A.M. Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn Affect Behav Neurosci 2001, 1(4):371-381.
30. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992, 106(2):274-285.
31. Yap C.S., Richardson R. Extinction in the developing rat: an examination of renewal effects. Dev Psychobiol 2007, 49(6):565-575.
32. Kim J.H., Richardson R. Immediate post-reminder injection of gamma-amino butyric acid (GABA) agonist midazolam attenuates reactivation of forgotten fear in the infant rat. Behav Neurosci 2007, 121(6):1328-1332.
33. Kim J.H., Richardson R. A developmental dissociation of context and GABA effects on extinguished fear in rats. Behav Neurosci 2007, 121(1):131-139.
34. Bouton M.E., et al. Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol Psychiatry 2006, 60(4):352-360.
35. Barad M., Gean P.W., Lutz B. The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 2006, 60(4):322-328.
36. Quirk G.J., Garcia R., Gonzalez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 2006, 60(4):337-343.
37. Agis-Balboa R.C., et al. A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. EMBO J 2011, 30(19):4071-4083.
38. McDonald H.Y., Wojtowicz J.M. Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci Lett 2005, 385(1):70-75.
39. Heine V.M., et al. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 2004, 25(3):361-375.
40. He J., Crews F.T. Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav 2007, 86(2):327-333.
41. Cowen D.S., et al. Age-dependent decline in hippocampal neurogenesis is not altered by chronic treatment with fluoxetine. Brain Res 2008, 1228:14-19.
42. Leranth C., Petnehazy O., MacLusky N.J. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J Neurosci 2003, 23(5):1588-1592.
43. Jernigan T.L., et al. Maturation of human cerebrum observed in vivo during adolescence. Brain 1991, 114(Pt 5):2037-2049.
44. Giedd J.N., et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999, 2(10):861-863.
45. Sowell E.R., et al. In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 1999, 2(10):859-861.
46. Markham J.A., Morris J.R., Juraska J.M. Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 2007, 144(3):961-968.
47. Casey B.J., Giedd J.N., Thomas K.M. Structural and functional brain development and its relation to cognitive development. Biol Psychol 2000, 54(1-3):241-257.
48. Sowell E.R., et al. Improved memory functioning and frontal lobe maturation between childhood and adolescence: a structural MRI study. J Int Neuropsychol Soc 2001, 7(3):312-322.
49. Kritzer M.F., et al. Gonadectomy impairs T-maze acquisition in adult male rats. Horm Behav 2001, 39(2):167-174.
50. Kritzer M.F., et al. Effects of gonadectomy on performance in operant tasks measuring prefrontal cortical function in adult male rats. Horm Behav 2007, 51(2):183-194.
51. Gibbs R.B. Testosterone and estradiol produce different effects on cognitive performance in male rats. Horm Behav 2005, 48(3):268-277.
52. Kulkarni S.K., Sharma A.C. Elevated plus-maze: a novel psychobehavioral tool to measure anxiety in rodents. Methods Find Exp Clin Pharmacol 1991, 13(8):573-577.
53. Itoh J., Nabeshima T., Kameyama T. Utility of an elevated plus-maze for dissociation of amnesic and behavioral effects of drugs in mice. Eur J Pharmacol 1991, 194(1):71-76.
54. Alexander J.C., et al. The role of calsenilin/DREAM/KChIP3 in contextual fear conditioning. Learn Mem 2009, 16(3):167-177.