Chronic anabolic androgenic steroid exposure alters corticotropin releasing factor expression and anxiety-like behaviors in the female mouse

Psychoneuroendocrinology

Volumn 35, Issue 10, 2010, Pages 1473-1485

  Costine, Beth A ^a   Oberlander, Joseph G ^a   Davis, Matthew C ^a   Penatti, Carlos A A ^a   Porter, Donna M ^a   Leaton, Robert N ^b   Henderson, Leslie P ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b Dartmouth College   (United States)

Author keywords

Anabolic; Anxiety; CRF; Extended amygdala; Mouse; Startle; Steroid

Indexed keywords

ANABOLIC AGENT; ANDROGEN; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; MESSENGER RNA; METANDIENONE; NANDROLONE DECANOATE; STEROID; TESTOSTERONE CIPIONATE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BODY IMAGE; BODY MASS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DRUG EXPOSURE; FEAR; FEMALE; GRIP STRENGTH; HABITUATION; HORMONE RELEASE; IMMUNOREACTIVITY; MEDIAN EMINENCE; MOUSE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY GATING; STARTLE REFLEX; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS;

AMYGDALA; ANABOLIC AGENTS; ANDROGENS; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; FEAR; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; IMMUNOHISTOCHEMISTRY; METHANDROSTENOLONE; MICE; MICE, INBRED C57BL; NANDROLONE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEPTAL NUCLEI; STARTLE REACTION; STEROIDS;

EID: 78650172139     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2010.04.015     Document Type: Article

References (115)

1. Adamec R.E., Blundell J., Collins A. Neural plasticity and stress induced changes in defense in the rat. Neurosci. Biobehav. Rev. 2001, 25:721-744.
2. Agis-Balboa R.C., Pibiri F., Nelson M., Pinna G. Enhanced fear responses in mice treated with anabolic androgenic steroids. Neuroendocrinology 2009, 20:617-621.
3. Ågren G., Thiblin I., Tirassa P., Lundeberg T., Stenfors C. Behavioural anxiolytic effects of low-dose anabolic androgenic steroid treatment in rats. Physiol. Behav. 1999, 66:503-509.
4. Ahima R.S., Harlan R.E. Regulation of glucocorticoid receptor immunoreactivity in the rat hippocampus by androgenic-anabolic steroids. Brain Res. 1992, 585:311-314.
5. Ambar G., Chiavegatto S. Anabolic-androgenic steroid treatment induces behavioral disinhibition and downregulation of serotonin receptor messenger RNA in the prefrontal cortex and amygdala of male mice. Genes Brain Behav. 2009, 8:161-173.
6. Asan E., Yilmazer-Hanke D.M., Eliava M., Hantsch M., Lesch K.P., Schmitt A. The corticotrophin-releasing factor (CRF)-system and monoaminergic afferents in the central amygdala: investigations in different mouse strains and comparison in the rat. Neuroscience 2005, 131:953-967.
7. Bahrke M.S., Yesalis C.E., Kopstein A.N., Stephens J.A. Risk factors associated with anabolic-androgenic steroid use among adolescents. Sports Med. 2000, 29:397-405.
8. Bahrke M.S., Yesalis C.E., Wright J.E. Psychological and behavioural effects of endogenous testosterone and anabolic-androgenic steroids. An update. Sports Med. 1996, 22:367-390.
9. Bajo M., Cruz M.T., Siggins G.R., Messing R., Roberto M. Protein kinase C epsilon mediation of CRF- and ethanol-induced GABA release in central amygdala. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8410-8415.
10. Bale T.L., Vale W.W. CRF and CRF receptors: Role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 2004, 44:525-557.
11. Barreto-Estrada J.L., Barreto J., Fortis-Santiago Y., Rivera-Ramos I., Fortis-Santiago A., Jorge J.C. Modulation of affect after chronic exposure to the anabolic steroid 17α-methyltestosterone in adult mice. Behav. Neurosci. 2004, 118:1071-1079.
12. Basaria S., Wahlstrom J.T., Dobs A.S. Clinical review 138: anabolic-androgenic steroid therapy in the treatment of chronic diseases. J. Clin. Endocrinol. Metab. 2001, 86:5108-5117.
13. A receptors in the rat. Horm. Behav. 1993, 27:568-583.
14. Blasberg M.E., Clark A.S. Anabolic-androgenic steroid effects on sexual receptivity in ovariectomized rats. Horm. Behav. 1997, 32:201-208.
15. Casu M.A., Pisu C., Lobina C., Pani L. Immunocytochemical study of the forebrain serotonergic innervation in Sardinian alcohol-preferring rats. Psychopharmacology 2004, 172:341-351.
16. Clark A.S., Barber D.M. Anabolic-androgenic steroids and aggression in adult castrated male rats. Physiol. Behav. 1994, 55(5):1107-1113.
17. Clark A.S., Costine B.A., Jones B.L., Kelton-Rehkopf M.C., Meerts S.H., Nutbrown-Greene L.L., Penatti C.A.A., Porter D.M., Yang P., Henderson L.P. Sex- and age-specific effects of anabolic androgenic steroids on reproductive behaviors and on GABAergic transmission in neuroendocrine control regions. Brain Res. 2006, 1126:122-138.
18. Clark A.S., Henderson L.P. Behavioral and physiological responses to anabolic-androgenic steroids. Neurosci. Biobehav. Rev. 2003, 27:413-436.
19. Cooper R.L., Goldman J.M., Vandenbergh J.G. Monitoring of the estrous cycle in the laboratory rodent by vaginal lavage. Methods in Toxicology 1993, 45-55. Academic Press, New York. J.J. Heindel, R.E. Chapin (Eds.).
20. Crawley J.N. What's Wrong with My Mouse? Behavioral Phenotying of Transgenic and Knockout Mice 2000, Wiley-Liss, New York, NY USA, pp. 54-55.
21. Daly R.C., Su T.P., Schmidt P.J., Pickar D., Murphy D.L., Rubinow D.R. Cerebrospinal fluid and behavioral changes after methyltestosterone administration: preliminary findings. Arch. Gen. Psychiatry 2001, 58:172-177.
22. Davis M. Neural systems involved in fear and anxiety measured with fear-potentiated startle. Am. Psychol. 2006, 61:741-756.
23. Davis M., Walker D.L., Miles L., Grillon C. Phasic vs. sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010, 35:105-135.
24. Davis M., Whalen P.J. The amygdala: vigilance and emotion. Mol. Psychiarty 2001, 6:13-34.
25. Day H.E.W., Curran E.J., Watson S.J., Akil H. Distinct neurochemical populations in the rat central nucleus of the amygdala and bed nucleus of the stria terminalis: evidence for their selective activation by interleukin-1β. J. Comp. Neurol. 1999, 413:113-128.
26. DuRant R.H., Rickert V.I., Ashworth C.S., Newman C., Slavens G. Use of multiple drugs among adolescents who use anabolic steroids. N. Engl. J. Med. 1993, 328:922-926.
27. Elliot D.L., Cheong J.W., Moe E.L., Goldberg L. Cross-sectional study of female students reporting anabolic steroid use. Arch. Pediatr. Adolesc. Med. 2007, 161:572-577.
28. Falls W.A., Carlson S., Turner J.G., Willott J.F. Fear-potentiated startle in two strains of inbred mice. Behav. Neurosci. 1997, 111:855-861.
29. Franke W.W., Berendonk B. Hormonal doping and androgenization of athletes: a secret program of the German Democratic Republic government. Clin. Chem. 1997, 43:1262-1279.
30. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego, CA.
31. Geyer M.A., McIlwain K.L., Paylor R. Mouse genetic models for prepulse inhibition: an early review. Mol. Psychiatry 2002, 7:1039-1053.
32. Graham M.R., Davies B., Grace F.M., Kicman A., Baker J.S. Anabolic steroid use: patterns of use and detection of doping. Sports Med. 2008, 38:505-525.
33. Gruber A.J., Pope H.G. Psychiatric and medical effects of anabolic-androgenic steroid use in women. Psychother. Psychosom. 2000, 69:19-26.
34. A receptor-mediated transmission in the hypothalamus: Effects on reproductive function. Neuropharmacology 2007, 52:1439-1453.
35. Henderson L.P., Penatti C.A.A., Jones B.L., Yang P., Clark A.S. Anabolic androgenic steroids and forebrain GABAergic transmission. Neuroscience 2006, 138:793-799.
36. Herman J.P., Tasker J.G., Ziegler D.R., Cullinan W.E. Local circuit regulation of paraventricular nucleus stress integration Glutamate-GABA connections. Pharmacol. Biochem. Behav. 2002, 71:457-468.
37. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:1201-1213.
38. Holsboer F., Ising M. Central CRH system in depression and anxiety-evidence from clinical studies with CRH1 receptor antagonists. Eur. J. Pharmacol. 2008, 583:350-357.
39. Jaferi A., Lane D.A., Pickel V.M. Subcellular plasticity of the corticotropin-releasing factor receptor in dendrites of the mouse bed nucleus of the stria terminalis following chronic opiate exposure. Neuroscience 2009, 163:143-154.
40. Johnston, L.D., O'Malley, P.M., Bachman, J.G., Schulenberg, J.E., 2009. Monitoring the Future national survey results on drug use, 1975-2008, vol. I: Secondary school students (NIH Publication No. 09-7402). National Institute on Drug Abuse, Bethesda, MD, 721 pp.
41. Kanayama G., Hudson J.I., Pope H.G. Long-term psychiatric and medical consequences of anabolic-androgenic steroid abuse: a looming public health concern?. Drug Alcohol Depend. 2008, 98:1-12.
42. Kash T.L., Winder D.G. Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis. Neuropharmacology 2006, 51:1013-1022.
43. Kerr J.M., Congeni J.A. Anabolic-androgenic steroids: use and abuse in pediatric patients. Pediatr. Clin. North Am. 2007, 54:771-785. xii.
44. Kibble M.W., Ross M.B. Adverse effects of anabolic steroids in athletes. Clin. Pharm. 1987, 6:686-692.
45. Kindlundh A.M.S., Isacson D.G.L., Berglund L., Nyberg F. Factors associated with adolescent use of doping agents: anabolic-androgenic steroids. Addiction 1999, 94:543-553.
46. Koch M. The neurobiology of startle. Prog. Neurobiol. 1999, 59:107-128.
47. Koob G.F. Brain stress systems in the amygdala and addiction. Brain Res. 2009, 1293:61-75.
48. Koob G.F., Heinrichs S.C. A role for corticotropin releasing factor and urocortin in behavioral responses to stressors. Brain Res. 1999, 848:141-152.
49. Korosi A., Baram T.Z. The central corticotropin releasing factor system during development and adulthood. Eur. J. Pharmacol. 2008, 583:204-214.
50. Kouvelas D., Pourzitaki C., Papazisis G., Dagklis T., Dimou K., Kraus M.M. Nandrolone abuse decreases anxiety and impairs memory in rats via central androgenic receptors. Int. J. Neuropsychopharmacol. 2008, 11:925-934.
51. Kuhn C.M. Anabolic steroids. Recent Prog. Horm. Res. 2002, 57:411-434.
52. Kutscher E.C., Lund B.C., Perry P.J. Anabolic steroids: a review for the clinician. Sports Med. 2002, 32:285-296.
53. Laviola G., Adriani W., Morley-Fletcher S., Terranova M.L. Peculiar response of adolescent mice to acute and chronic stress and to amphetamine: evidence of sex differences. Behav. Brain Res. 2002, 130:117-125.
54. Lee Y., Davis M. Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle response. J. Neurosci. 1997, 17:6434-6446.
55. Lee Y., Fitz S., Johnson P.L., Shekhar A. Repeated stimulation of CRF receptors in the BNST of rats selectively induces social but not panic-like anxiety. Neuropsychopharmacology 2008, 33:2586-2594.
56. Liang K.C., Melia K.R., Miserendino M.J.D., Falls W.A., Campeau S., Davis M. Corticotropin-releasing factor: long-lasting facilitation of the acoustic startle reflex. J. Neurosci. 1992, 12:2302-2312.
57. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2T-ΔΔC Method. Methods 2001, 25:402-408.
58. Llewellyn W. Anabolics 2007, Body of Science, Jupiter, FL. 6th ed.
59. Matrisciano F., Modafferi A.M.E., Togna G.I., Barone Y., Pinna G., Nicoletti F., Scaccianoce S. Repeated anabolic androgenic steroid treatment causes anti-depressant-reversible alterations of the hypothalamic-pituitary-adrenal axis, BDNF levels and behavior. Neuropharmacology 2010, 58:1078-1084.
60. Matsumoto A.M., Bremner W.J. Serum testosterone assays-accuracy matters. J. Clin. Endocrinol. Metab. 2004, 89:520-524.
61. Miller K.E., Hoffman J.H., Barnes G.M., Sado D., Melnick M.J., Farrell M.P. Adolescent anabolic steroid use, gender, physical activity, and other problem behaviors. Subst. Use Misuse 2005, 40:1637-1657.
62. Minkin D.M., Meyer M.E., van Haaren F. Behavioral effects of long-term administration of an anabolic steroid in intact and castrated male Wistar rats. Pharmacol. Biochem. Behav. 1993, 44:959-963.
63. Nie Z., Schweitzer P., Roberts A.J., Madamba S.G., Moore S.D., Siggins G.R. Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 2004, 303:1512-1514.
64. 1 receptors mediate the ethanol enhancement of GABAergic transmission in the mouse central amygdala. Sci. World J. 2009, 9:68-85.
65. Nilsson S., Baigi A., Marklund B., Fridlund B. The prevalence of the use of androgenic anabolic steroids by adolescents in a county of Sweden. Eur. J. Public Health 2001, 11:195-197.
66. O'Connor L.H., Cicero T.J. Anabolic steroids: misuse or abuse?. Hormonally Induced Changes in Mind and Brain 1993, 129-156. Academic Press, San Diego, CA. J. Schulkin (Ed.).
67. Oorschot D.E. Are you using neuronal densities, synaptic densities or neurochemical densities as your definitive data? There is a better way to go. Prog. Neurobiol. 1994, 44:233-247.
68. Owens M.J., Nemeroff C.B. Physiology and pharmacology of corticotropin-releasing factor. Pharmacol. Rev. 1991, 43:425-473.
69. Pagonis T.A., Angelopoulos N.V., Koukoulis G.N., Hadjichristodoulou C.S. Psychiatric side effects induced by supraphysiological does of combinations of anabolic steroids correlate to the severity of abuse. Eur. Psychiatry 2006, 21:551-562.
70. Pallesen S., Jøsendal O., Johnsen B.H., Larsen S., Molde H. Anabolic steroid use in high school students. Subst. Use Misuse 2006, 41:1705-1717.
71. Peirson S.N., Butler J.N., Foster R.G. Experimental validation of novel and conventional approaches to quantitative real-time PCR data analysis. Nucleic Acids Res. 2003, 31:e73.
72. 5-receptor mediated GABAergic transmission and neural signaling in the forebrain of female mice. Neuroscience 2009, 161:526-537.
73. A receptor-mediated synaptic transmission disrupts the firing of gonadotropin-releasing hormone neurons in male mice under conditions of steroid abuse. J. Neurosci. 2010, 30(19):6497-6506.
74. Penatti C.A.A., Porter D.M., Henderson L.P. Chronic exposure to anabolic androgenic steroids alters neuronal function in the mammalian forebrain via androgen receptor- and estrogen receptor-mediated mechanisms. J. Neurosci. 2009, 29:12484-12496.
75. A receptor expression and function in adolescent mice. Neuroscience 2005, 135:533-543.
76. Perry P.J., Andersen K.H., Yates W.R. Illicit anabolic steroid use in athletes. Am. J. Sports Med. 1990, 18:422-428.
77. Perry P.J., Kutscher E.C., Lund B.C., Yates W.R., Holman T.L., Demers L. Measures of aggression and mood changes in male weight lifters with and without androgenic anabolic steroid use. J. Forensic Sci. 2003, 48:646-651.
78. Peterson R.S., Yarram L., Schlinger B.A., Saldanha C.J. Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc. Biol. Sci. 2005, 272:2089-2096.
79. Pinna G., Agis-Balboa R.C., Pibiri F., Nelson M., Guidotti A., Costa E. Neurosteroid biosynthesis regulates sexually dimorphic fear and aggressive behavior in mice. Neurochem. Res. 2008, 33:199-2007.
80. Pibiri F., Nelson M., Carboni G., Pinna G. Neurosteroids regulate mouse aggression induced by anabolic androgenic steroids. Neuroreport 2006, 17:1537-1541.
81. Pibiri F., Nelson M., Guidotti A., Costa E., 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.
82. Plappert C.F., Pilz P.K.D., Schnitzler H.-U. Acoustic startle response and habituation in freezing and nonfreezing rats. Behav. Neurosci. 1993, 107:981-987.
83. Pope H.G., Katz D.L. Affective and psychotic symptoms associated with anabolic steroid use. Am. J. Psychiatry 1988, 145:487-490.
84. Pope H.G., Kouri E.M., Hudson J.I. Effects of supraphysiologic doses of testosterone on mood and aggression in normal men. Arch. Gen. Psychiatry 2000, 57:133-140.
85. Regan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies. FABSB J. 2007, 22:659-661.
86. Reul J.M.H.M., Holsboer F. Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Curr. Opin. Pharmacol. 2002, 2:23-33.
87. Risbrough V.B., Geyer M.A. Anxiogenic treatments do not increase fear-potentiated startle in mice. Biol. Psychiatry 2005, 57:33-43.
88. Risbrough V.B., Hauger R.L., Pelleymounter M.A., Geyer M.A. Role of corticotropin releasing factor (CRF) receptors 1 and 2 in CRF-potentiated acoustic startle in mice. Psychopharmacology 2003, 170:178-187.
89. 2 exert both additive and opposing influences on defensive startle behavior. J. Neurosci. 2004, 24:6545-6552.
90. Roberto M., Cruz M.T., Gilpin N.W., Sabino V., Schweitzer P., Bajo M., Cottone P., Madamba S.G., Stouffer D.G., Zorrilla E.P., Koob G.F., Siggins G.R., Pasrons L.H. Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence. Biol. Psychiatry 2010, January 6 [Epub ahead of print].
91. Rocha V.M., Calil C.M., Ferreira R., Moura M.J.C.S., Marcondes F.K. Influence of anabolic steroid on anxiety levels in sedentary male rats. Stress 2007, 10:326-331.
92. Rojas-Ortiz Y.A., Rundle-Gonzalez V., Rivera-Ramos I., Jorge J.C. Modulation of elevated plus maze behavior after chronic exposure to the anabolic steroid 17α-methyltestosterone in adult mice. Horm. Behav. 2006, 49:123-128.
93. Ryan K.J. Biological aromatization of steroids. J. Biol. Chem. 1959, 234:268-272.
94. Sakanaka M., Shibasaki T., Lederis K. Distibution and efferent projections of corticoptropin-releasing factor-like immunoreactivity in the rat amygdaloid complex. Brain Res. 1986, 382:213-238.
95. Sato S.M., Schulz K.M., Sisk C.L., Wood R.I. Adolescents and androgens, receptors and rewards. Horm. Behav. 2008, 53:647-658.
96. Schlussman S.D., Zhou Y., Johansson P., Kiuru A., Ho A., Nyberg F., Kreek M.J. Effects of the androgenic anabolic steroid, nandrolone decanoate, on adrenocorticotropin hormone, corticosterone and proopiomelanocortin, corticotropin releasing factor (CRF) and CRF receptor1 mRNA levels in the hypothalamus, pituitary and amygdala of the rat. Neurosci. Lett. 2000, 284:190-194.
97. Silberman Y., Bajo M., Chappell A.M., Christian D.T., Cruz M., Diaz M.R., Kash T., Lack A.K., Messing R.O., Siggins G.R., Winder D., Roberto M., McCool B.A., Weiner J.L. Neurobiological mechanisms contributing to alcohol-stress-anxiety interactions. Alcohol 2009, 43:509-519.
98. Steensland P., Blakely G., Nyberg F., Fahlke C., Pohorecky L.A. Anabolic androgenic steroid affects social aggression and fear-related behaviors in male pair-housed rats. Horm. Behav. 2005, 48:216-224.
99. Sturmi J.E., Diorio D.J. Anabolic agents. Clin. Sports Med. 1998, 17:261-282.
100. Su T.P., Pagliaro M., Schmidt P.J., Pickar D., Wolkowitz O., Rubinow D.R. Neuropsychiatric effects of anabolic steroids in male normal volunteers. JAMA 1993, 269:2760-2764.
101. Sun N., Cassell M.D. Intrinsic GABAergic neurons in the rat central extended amygdala. J. Comp. Neurol. 1993, 330:381-404.
102. Swerdlow N.R., Britton K.T., Koob G.F. Potentiation of acoustic startle by corticotropin-releasing factor (CRF) and by fear are both reversed by α-helical CRF (9-41). Neuropsychopharmacology 1989, 2:285-292.
103. Swerdlow N.R., Geyer M.A., Vale W.W., Koob G.F. Corticotropin-releasing factor potentiates acoustic startle in rats: blockade by chlordiazepoxide. Psychopharmacology 1986, 88:147-152.
104. Trenton A.J., Currier G.W. Behavioural manifestations of anabolic steroid use. CNS Drugs 2005, 19:571-595.
105. van Pett K., Viau V., Bittencourt J.C., Chan R.K.W., Li H.Y., Arias C., Prins G.S., Perrin M., Vale W., Sawchenko P.E. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 2000, 428:191-212.
106. Veinante P., Stoeckel M.E., Freund-Mercier M.J. GABA- and peptide-immunoreactivities co-localize in the rat central extended amygdala. Neuroreport 1997, 8:2985-2989.
107. Walker D.L., Miles L.A., Davis M. Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:1291-1308.
108. Walker D., Yang Y., Ratti E., Corsi M., Trist D., Davis M. Differential effects of the CRF-R1 antagonist GSK876008 on fear-potentiated, light- and CRF-enhanced startle suggest preferential involvement in sustained vs. phasic threat responses. Neuropsychopharmacology 2009, 34:1533-1542.
109. Willott J.F., Carlson S. Modification of the acoustic startle response in hearing-impaired C57Bl/6J mice: prepulse augmentation and prolongation of prepulse inhibition. Behav. Neurosci. 1995, 109:396-403.
110. Willott J.F., Carlson S., Chen H. Prepulse inhibition of the startle response in mice: relationship to hearing loss and auditory system plasticity. Behav. Neurosci. 1994, 108:703-713.
111. Willott J.F., Tanner L., O'Steen J., Johnson K.R., Bogue M.A., Gagnon L. Acoustic startle and prepulse inhibition in 40 inbred strains of mice. Behav. Neurosci. 2003, 117:716-727.
112. Winters S. Androgens: endocrine physiology and pharmacology. NIDA Res. Monographs 1990, 102:113-130.
113. Wu F.C. Endocrine aspects of anabolic steroids. Clin. Chem. 1997, 43:1289-1292.
114. Yesalis C.E., Barsukiewicz C.K., Kopstein A.N., Bahrke M.S. Trends in anabolic-androgenic steroid use among adolescents. Arch. Pediatr. Adolesc. Med. 1997, 151:1197-1206.
115. Zender R., Olshansky E. Women's mental health: depression and anxiety. Nurs. Clin. North Am. 2009, 44:355-364.