Sex differences in anxiety disorders: Interactions between fear, stress, and gonadal hormones

Hormones and Behavior

Volumn 76, Issue , 2015, Pages 106-117

  Maeng, Lisa Y ^a   Milad, Mohammed R ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Anxiety; Estrogen; Fear conditioning; Fear extinction; Progesterone; Psychiatric disorders; PTSD; Sex difference; Stress; Testosterone

Indexed keywords

ANTIDEPRESSANT AGENT; ESTROGEN; FLUOXETINE; PROGESTERONE; TESTOSTERONE; SEX HORMONE;

ANXIETY DISORDER; ARTICLE; BRAIN REGION; DISEASE ASSOCIATION; FEAR; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MEMORY CONSOLIDATION; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; SEX DIFFERENCE; STRESS; TASK PERFORMANCE; FEMALE; MALE; MENTAL STRESS; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANXIETY DISORDERS; FEAR; FEMALE; GONADAL HORMONES; HUMANS; MALE; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 84947865344     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.04.002     Document Type: Article

References (217)

1. Aguilar R., Gil L., Gray J.A., Driscoll P., Flint J., Dawson G.R., Tobeña A. Fearfulness and sex in F2 Roman rats: males display more fear though both sexes share the same fearfulness traits. Physiol. Behav. 2003, 78(4-5):723-732. 10.1016/S0031-9384(03)00043-X.
2. Akirav I., Maroun M. The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plast. 2007, 2007:30873. 10.1155/2007/30873.
3. Altemus M., Sarvaiya N., Neill Epperson C. Sex differences in anxiety and depression clinical perspectives. Front. Neuroendocrinol. 2014, 35(3):320-330. 10.1016/j.yfrne.2014.05.004.
4. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2013, Author, Washington, D.C. 5th ed.
5. Anagnostaras S.G., Maren S., DeCola J.P., Lane N.I., Gale G.D., Schlinger B.A., Fanselow M.S. 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.
6. Andreano J.M., Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. NeuroImage 2010, 53(4):1286-1293. 10.1016/j.neuroimage.2010.07.011.
7. Antov M.I., Stockhorst U. Stress exposure prior to fear acquisition interacts with estradiol status to alter recall of fear extinction in humans. Psychoneuroendocrinology 2014, 49:106-118. 10.1016/j.psyneuen.2014.06.022.
8. Arnold A.P., Breedlove S.M. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm. Behav. 1985, 19(4):469-498.
9. Arnsten A.F. Catecholamine regulation of the prefrontal cortex. J. Psychopharmacol. 1997, 11(2):151-162.
10. Arnsten A.F.T. Stress signalling pathways that impair prefrontal cortex structure and function. Nat. Rev. Neurosci. 2009, 10(6):410-422. 10.1038/nrn2648.
11. Bäckström T., Bixo M., Johansson M., Nyberg S., Ossewaarde L., Ragagnin G., van Wingen G. Allopregnanolone and mood disorders. Prog. Neurobiol. 2014, 113:88-94. 10.1016/j.pneurobio.2013.07.005.
12. Baker-Andresen D., Flavell C.R., Li X., Bredy T.W. Activation of BDNF signaling prevents the return of fear in female mice. Learn. Mem. 2013, 20(5):237-240. 10.1101/lm.029520.112.
13. Bakish D. The patient with comorbid depression and anxiety: the unmet need. J. Clin. Psychiatry 1999, 60(Suppl. 6):20-24.
14. Bangasser D.A., Shors T.J. Critical brain circuits at the intersection between stress and learning. Neurosci. Biobehav. Rev. 2010, 34(8):1223-1233. 10.1016/j.neubiorev.2010.02.002.
15. Bangasser D.A., Santollo J., Shors T.J. The bed nucleus of the stria terminalis is critically involved in enhancing associative learning after stressful experience. Behav. Neurosci. 2005, 119(6):1459-1466. 10.1037/0735-7044.119.6.1459.
16. Baran S.E., Armstrong C.E., Niren D.C., Hanna J.J., Conrad C.D. Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol. Learn. Mem. 2009, 91(3):323-332. 10.1016/j.nlm.2008.11.005.
17. Baran S.E., Armstrong C.E., Niren D.C., Conrad C.D. Prefrontal cortex lesions and sex differences in fear extinction and perseveration. Learn. Mem. 2010, 17(5):267-278. 10.1101/lm.1778010.
18. Barha C.K., Dalton G.L., Galea L.A. Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats. Neuropsychopharmacology 2010, 35(2):547-559. 10.1038/npp.2009.161.
19. Bentz D., Michael T., Wilhelm F.H., Hartmann F.R., Kunz S., von Rohr I.R.R., de Quervain D.J.-F. Influence of stress on fear memory processes in an aversive differential conditioning paradigm in humans. Psychoneuroendocrinology 2013, 38(7):1186-1197. 10.1016/j.psyneuen.2012.12.018.
20. Biggio G., Pisu M.G., Biggio F., Serra M. Allopregnanolone modulation of HPA axis function in the adult rat. Psychopharmacology 2014, 231(17):3437-3444. 10.1007/s00213-014-3521-6.
21. Bishop S.J. Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn. Sci. 2007, 11(7):307-316. 10.1016/j.tics.2007.05.008.
22. Bremner J.D., Randall P., Vermetten E., Staib L., Bronen R.A., Mazure C., Charney D.S. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse-a preliminary report. Biol. Psychiatry 1997, 41(1):23-32.
23. Breslau N. Gender differences in trauma and posttraumatic stress disorder. J. Gend. Specif. Med. 2002, 5(1):34-40.
24. Breslau N. The epidemiology of trauma, PTSD, and other posttrauma disorders. Trauma Violence Abuse 2009, 10(3):198-210. 10.1177/1524838009334448.
25. Breslau N., Davis G.C., Andreski P., Peterson E.L., Schultz L.R. Sex differences in posttraumatic stress disorder. Arch. Gen. Psychiatry 1997, 54(11):1044-1048.
26. Breslau N., Kessler R.C., Chilcoat H.D., Schultz L.R., Davis G.C., Andreski P. Trauma and posttraumatic stress disorder in the community: the 1996 Detroit Area Survey of Trauma. Arch. Gen. Psychiatry 1998, 55(7):626-632.
27. Briscione M.A., Jovanovic T., Norrholm S.D. Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors. Front. Psychiatry 2014, 5:88. 10.3389/fpsyt.2014.00088.
28. Brummelte S., Galea L.A.M. Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm. Behav. 2010, 58(5):769-779. 10.1016/j.yhbeh.2010.07.012.
29. Campbell-Sills L., Barlow D.H., Brown T.A., Hofmann S.G. Acceptability and suppression of negative emotion in anxiety and mood disorders. Emotion 2006, 6(4):587-595. 10.1037/1528-3542.6.4.587.
30. Chang Y.-J., Yang C.-H., Liang Y.-C., Yeh C.-M., Huang C.-C., Hsu K.-S. Estrogen modulates sexually dimorphic contextual fear extinction in rats through estrogen receptor beta. Hippocampus 2009, 19(11):1142-1150. 10.1002/hipo.20581.
31. Chen L.-S., Tzeng W.-Y., Chuang J.-Y., Cherng C.G., Gean P.-W., Yu L. Roles of testosterone and amygdaloid LTP induction in determining sex differences in fear memory magnitude. Horm. Behav. 2014, 66(3):498-508. 10.1016/j.yhbeh.2014.07.008.
32. Coffey C.E., Wilkinson W.E., Weiner R.D., Parashos I.A., Djang W.T., Webb M.C., Spritzer C.E. Quantitative cerebral anatomy in depression. A controlled magnetic resonance imaging study. Arch. Gen. Psychiatry 1993, 50(1):7-16.
33. Cook S.C., Wellman C.L. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J. Neurobiol. 2004, 60(2):236-248. 10.1002/neu.20025.
34. Corcoran K.A., Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J. Neurosci. Off. J. Soc. Neurosci. 2001, 21(5):1720-1726.
35. Cover K.K., Maeng L.Y., Lebrón-Milad K., Milad M.R. Mechanisms of estradiol in fear circuitry: implications for sex differences in psychopathology. Transl. Psychiatry 2014, 4:e422. 10.1038/tp.2014.67.
36. Dalla C., Pitychoutis P.M., Kokras N., Papadopoulou-Daifoti Z. Sex differences in animal models of depression and antidepressant response. Basic Clin. Pharmacol. Toxicol. 2010, 106(3):226-233. 10.1111/j.1742-7843.2009.00516.x.
37. Damoiseaux V.A., Proost J.H., Jiawan V.C.R., Melgert B.N. Sex differences in the pharmacokinetics of antidepressants: influence of female sex hormones and oral contraceptives. Clin. Pharmacokinet. 2014, 53(6):509-519. 10.1007/s40262-014-0145-2.
38. Daviu N., Andero R., Armario A., Nadal R. Sex differences in the behavioural and hypothalamic-pituitary-adrenal response to contextual fear conditioning in rats. Horm. Behav. 2014, 66(5):713-723. 10.1016/j.yhbeh.2014.09.015.
39. De Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394(6695):787-790. 10.1038/29542.
40. Dias B.G., Banerjee S.B., Goodman J.V., Ressler K.J. Towards new approaches to disorders of fear and anxiety. Curr. Opin. Neurobiol. 2013, 23(3):346-352. 10.1016/j.conb.2013.01.013.
41. DiBlasio C.J., Hammett J., Malcolm J.B., Judge B.A., Womack J.H., Kincade M.C., Derweesh I.H. Prevalence and predictive factors for the development of de novo psychiatric illness in patients receiving androgen deprivation therapy for prostate cancer. Can. J. Urol. 2008, 15(5):4249-4256. (discussion 4256).
42. Dismukes A.R., Johnson M.M., Vitacco M.J., Iturri F., Shirtcliff E.A. Coupling of the HPA and HPG axes in the context of early life adversity in incarcerated male adolescents. Dev. Psychobiol. 2014, 10.1002/dev.21231.
43. Du X., Pang T.Y., Mo C., Renoir T., Wright D.J., Hannan A.J. The influence of the HPG axis on stress response and depressive-like behaviour in a transgenic mouse model of Huntington's disease. Exp. Neurol. 2014, 263C:63-71. 10.1016/j.expneurol.2014.09.009.
44. Ertman N., Andreano J.M., Cahill L. Progesterone at encoding predicts subsequent emotional memory. Learn. Mem. 2011, 18(12):759-763. 10.1101/lm.023267.111.
45. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatr. 2007, 164(10):1476-1488. 10.1176/appi.ajp.2007.07030504.
46. Fani N., King T.Z., Brewster R., Srivastava A., Stevens J.S., Glover E.M., Jovanovic T. Fear-potentiated startle during extinction is associated with white matter microstructure and functional connectivity. Cortex 2015, 64:249-259. 10.1016/j.cortex.2014.11.006.
47. Farrell M.R., Sengelaub D.R., Wellman C.L. Sex differences and chronic stress effects on the neural circuitry underlying fear conditioning and extinction. Physiol. Behav. 2013, 122:208-215. 10.1016/j.physbeh.2013.04.002.
48. Felmingham K., Williams L.M., Kemp A.H., Liddell B., Falconer E., Peduto A., Bryant R. Neural responses to masked fear faces: sex differences and trauma exposure in posttraumatic stress disorder. J. Abnorm. Psychol. 2010, 119(1):241-247. 10.1037/a0017551.
49. Fenchel D., Levkovitz Y., Vainer E., Kaplan Z., Zohar J., Cohen H. Beyond the HPA-axis: the role of the gonadal steroid hormone receptors in modulating stress-related responses in an animal model of PTSD. Eur. Neuropsychopharmacol. 2015, 10.1016/j.euroneuro.2015.02.004.
50. Fenton G.E., Pollard A.K., Halliday D.M., Mason R., Bredy T.W., Stevenson C.W. Persistent prelimbic cortex activity contributes to enhanced learned fear expression in females. Learn. Mem. 2014, 21(2):55-60. 10.1101/lm.033514.113.
51. Ferree N.K., Kamat R., Cahill L. Influences of menstrual cycle position and sex hormone levels on spontaneous intrusive recollections following emotional stimuli. Conscious. Cogn. 2011, 20(4):1154-1162. 10.1016/j.concog.2011.02.003.
52. Foa E.B. Psychosocial treatment of posttraumatic stress disorder. J. Clin. Psychiatry 2000, 61(Suppl. 5):43-48. (discussion 49-51).
53. Foa E.B. Prolonged exposure therapy: past, present, and future. Depress. Anxiety 2011, 28(12):1043-1047. 10.1002/da.20907.
54. Foa E.B., Street G.P. Women and traumatic events. J. Clin. Psychiatry 2001, 62(Suppl. 17):29-34.
55. Frackiewicz E.J., Sramek J.J., Cutler N.R. Gender differences in depression and antidepressant pharmacokinetics and adverse events. Ann. Pharmacother. 2000, 34(1):80-88.
56. Frans O., Rimmö P.-A., Aberg L., Fredrikson M. Trauma exposure and post-traumatic stress disorder in the general population. Acta Psychiatr. Scand. 2005, 111(4):291-299. 10.1111/j.1600-0447.2004.00463.x.
57. 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 ovariectomized rats. Behav. Neurosci. 2004, 118(2):306-313. 10.1037/0735-7044.118.2.306.
58. Frye C.A., Koonce C.J., Edinger K.L., Osborne D.M., Walf A.A. Androgens with activity at estrogen receptor beta have anxiolytic and cognitive-enhancing effects in male rats and mice. Horm. Behav. 2008, 54(5):726-734. 10.1016/j.yhbeh.2008.07.013.
59. Galvin C., Ninan I. Regulation of the mouse medial prefrontal cortical synapses by endogenous estradiol. Neuropsychopharmacology 2014, 39(9):2086-2094. 10.1038/npp.2014.56.
60. Garcia R., Vouimba R.M., Baudry M., Thompson R.F. The amygdala modulates prefrontal cortex activity relative to conditioned fear. Nature 1999, 402(6759):294-296. 10.1038/46286.
61. Garrett J.E., Wellman C.L. Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 2009, 162(1):195-207. 10.1016/j.neuroscience.2009.04.057.
62. Glover E.M., Jovanovic T., Mercer K.B., Kerley K., Bradley B., Ressler K.J., Norrholm S.D. Estrogen levels are associated with extinction deficits in women with posttraumatic stress disorder. Biol. Psychiatry 2012, 72(1):19-24. 10.1016/j.biopsych.2012.02.031.
63. Glover E.M., Mercer K.B., Norrholm S.D., Davis M., Duncan E., Bradley B., Jovanovic T. Inhibition of fear is differentially associated with cycling estrogen levels in women. J. Psychiatry Neurosci. 2013, 38(5):341-348. 10.1503/jpn.120129.
64. Glover E.M., Jovanovic T., Norrholm S.D. Estrogen and Extinction of Fear Memories: Implications for Posttraumatic Stress Disorder Treatment 2015, (in press). 10.1016/j.biopsych.2015.02.007.
65. Goel N., Workman J.L., Lee T.T., Innala L., Viau V. Sex differences in the HPA axis. Compr. Physiol. 2014, 4(3):1121-1155. 10.1002/cphy.c130054.
66. Goldstein J.M., Jerram M., Poldrack R., Ahern T., Kennedy D.N., Seidman L.J., Makris N. Hormonal cycle modulates arousal circuitry in women using functional magnetic resonance imaging. J. Neurosci. Off. J. Soc. Neurosci. 2005, 25(40):9309-9316. 10.1523/JNEUROSCI.2239-05.2005.
67. Goldstein J.M., Jerram M., Abbs B., Whitfield-Gabrieli S., Makris N. Sex differences in stress response circuitry activation dependent on female hormonal cycle. J. Neurosci. Off. J. Soc. Neurosci. 2010, 30(2):431-438. 10.1523/JNEUROSCI.3021-09.2010.
68. Graham B.M., Milad M.R. The study of fear extinction: implications for anxiety disorders. Am. J. Psychiatr. 2011, 168(12). 10.1176/appi.ajp.2011.11040557.
69. Graham B.M., Milad M.R. Blockade of estrogen by hormonal contraceptives impairs fear extinction in female rats and women. Biol. Psychiatry 2013, 73(4):371-378. 10.1016/j.biopsych.2012.09.018.
70. Graham B.M., Milad M.R. Inhibition of estradiol synthesis impairs fear extinction in male rats. Learn. Mem. 2014, 21(7):347-350. 10.1101/lm.034926.114.
71. Gray T.S., Bingaman E.W. The amygdala: corticotropin-releasing factor, steroids, and stress. Crit. Rev. Neurobiol. 1996, 10(2):155-168.
72. Gupta R.R., Sen S., Diepenhorst L.L., Rudick C.N., Maren S. Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats(1). Brain Res. 2001, 888(2):356-365.
73. Handa R.J., Weiser M.J. Gonadal steroid hormones and the hypothalamo-pituitary-adrenal axis. Front. Neuroendocrinol. 2014, 35(2):197-220. 10.1016/j.yfrne.2013.11.001.
74. Handa R.J., Burgess L.H., Kerr J.E., O'Keefe J.A. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm. Behav. 1994, 28(4):464-476. 10.1006/hbeh.1994.1044.
75. Hermans E.J., Putman P., Baas J.M., Koppeschaar H.P., van Honk J. A single administration of testosterone reduces fear-potentiated startle in humans. Biol. Psychiatry 2006, 59(9):872-874. 10.1016/j.biopsych.2005.11.015.
76. Hermans E.J., Putman P., Baas J.M., Gecks N.M., Kenemans J.L., van Honk J. Exogenous testosterone attenuates the integrated central stress response in healthy young women. Psychoneuroendocrinology 2007, 32(8-10):1052-1061. 10.1016/j.psyneuen.2007.08.006.
77. Hickey M., Bryant C., Judd F. Evaluation and management of depressive and anxiety symptoms in midlife. Climacteric 2012, 15(1):3-9. 10.3109/13697137.2011.620188.
78. Hiroi R., Neumaier J.F. Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behav. Brain Res. 2006, 166(1):93-100. 10.1016/j.bbr.2005.07.021.
79. Hodosy J., Zelmanová D., Majzúnová M., Filová B., Malinová M., Ostatníková D., Celec P. The anxiolytic effect of testosterone in the rat is mediated via the androgen receptor. Pharmacol. Biochem. Behav. 2012, 102(2):191-195. 10.1016/j.pbb.2012.04.005.
80. Hofmann S.G. Cognitive processes during fear acquisition and extinction in animals and humans: implications for exposure therapy of anxiety disorders. Clin. Psychol. Rev. 2008, 28(2):199-210. 10.1016/j.cpr.2007.04.009.
81. Holbrook T.L., Hoyt D.B., Stein M.B., Sieber W.J. Gender differences in long-term posttraumatic stress disorder outcomes after major trauma: women are at higher risk of adverse outcomes than men. J. Trauma 2002, 53(5):882-888. 10.1097/01.TA.0000033749.65011.6A.
82. Hyde J.S., Mezulis A.H., Abramson L.Y. The ABCs of depression: integrating affective, biological, and cognitive models to explain the emergence of the gender difference in depression. Psychol. Rev. 2008, 115(2):291-313. 10.1037/0033-295X.115.2.291.
83. Inagaki T., Gautreaux C., Luine V. Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm. Behav. 2010, 58(3):415-426. 10.1016/j.yhbeh.2010.05.013.
84. Inslicht S.S., Metzler T.J., Garcia N.M., Pineles S.L., Milad M.R., Orr S.P., Neylan T.C. Sex differences in fear conditioning in posttraumatic stress disorder. J. Psychiatr. Res. 2013, 47(1):64-71. 10.1016/j.jpsychires.2012.08.027.
85. Izquierdo A., Wellman C.L., Holmes A. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J. Neurosci. Off. J. Soc. Neurosci. 2006, 26(21):5733-5738. 10.1523/JNEUROSCI.0474-06.2006.
86. Jacobs E.G., Holsen L.M., Lancaster K., Makris N., Whitfield-Gabrieli S., Remington A., Weiss B., Buka S., Klibanski A., Goldstein J.M. 17β-estradiol differentially regulates stress circuitry activity in healthy and depressed women. Neuropsychopharmacology 2015, 40:566-576. 10.1038/npp.2014.203.
87. Jasnow A.M., Schulkin J., Pfaff D.W. Estrogen facilitates fear conditioning and increases corticotropin-releasing hormone mRNA expression in the central amygdala in female mice. Horm. Behav. 2006, 49(2):197-205. 10.1016/j.yhbeh.2005.06.005.
88. Kalisch R., Korenfeld E., Stephan K.E., Weiskopf N., Seymour B., Dolan R.J. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J. Neurosci. Off. J. Soc. Neurosci. 2006, 26(37):9503-9511. 10.1523/JNEUROSCI.2021-06.2006.
89. Kaltiala-Heino R., Kosunen E., Rimpelä M. Pubertal timing, sexual behaviour and self-reported depression in middle adolescence. J. Adolesc. 2003, 26(5):531-545.
90. Kanayama G., Amiaz R., Seidman S., Pope H.G. Testosterone supplementation for depressed men: current research and suggested treatment guidelines. Exp. Clin. Psychopharmacol. 2007, 15(6):529-538. 10.1037/1064-1297.15.6.529.
91. Keers R., Aitchison K.J. Gender differences in antidepressant drug response. Int. Rev. Psychiatry 2010, 22(5):485-500. 10.3109/09540261.2010.496448.
92. Kelly M.M., Forsyth J.P. Sex differences in response to an observational fear conditioning procedure. Behav. Ther. 2007, 38(4):340-349. 10.1016/j.beth.2006.10.007.
93. Kessler R.C., McGonagle K.A., Swartz M., Blazer D.G., Nelson C.B. Sex and depression in the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence. J. Affect. Disord. 1993, 29(2-3):85-96.
94. Kessler R.C., McGonagle K.A., Zhao S., Nelson C.B., Hughes M., Eshleman S., Kendler K.S. Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch. Gen. Psychiatry 1994, 51(1):8-19.
95. Kessler R.C., Sonnega A., Bromet E., Hughes M., Nelson C.B. Posttraumatic stress disorder in the National Comorbidity Survey. Arch. Gen. Psychiatry 1995, 52(12):1048-1060.
96. Kessler R.C., Chiu W.T., Demler O., Merikangas K.R., Walters E.E. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey replication. Arch. Gen. Psychiatry 2005, 62(6):617-627. 10.1001/archpsyc.62.6.617.
97. Kessler R.C., Chiu W.T., Jin R., Ruscio A.M., Shear K., Walters E.E. The epidemiology of panic attacks, panic disorder, and agoraphobia in the National Comorbidity Survey replication. Arch. Gen. Psychiatry 2006, 63(4):415-424. 10.1001/archpsyc.63.4.415.
98. Kessler R.C., Aguilar-Gaxiola S., Alonso J., Chatterji S., Lee S., Ormel J., Wang P.S. The global burden of mental disorders: an update from the WHO World Mental Health (WMH) surveys. Epidemiol. Psichiatr. Soc. 2009, 18(1):23-33.
99. Khakpai F. The effect of opiodergic system and testosterone on anxiety behavior in gonadectomized rats. Behav. Brain Res. 2014, 263:9-15. 10.1016/j.bbr.2014.01.013.
100. Kilpatrick D.G., Resnick H.S., Milanak M.E., Miller M.W., Keyes K.M., Friedman M.J. National estimates of exposure to traumatic events and PTSD prevalence using DSM-IV and DSM-5 criteria. J. Trauma. Stress. 2013, 26(5):537-547. 10.1002/jts.21848.
101. Kim H., Yi J.H., Choi K., Hong S., Shin K.S., Kang S.J. Regional differences in acute corticosterone-induced dendritic remodeling in the rat brain and their behavioral consequences. BMC Neurosci. 2014, 15:65. 10.1186/1471-2202-15-65.
102. Kirschbaum C., Schommer N., Federenko I., Gaab J., Neumann O., Oellers M., Hellhammer D.H. Short-term estradiol treatment enhances pituitary-adrenal axis and sympathetic responses to psychosocial stress in healthy young men. J. Clin. Endocrinol. Metab. 1996, 81(10):3639-3643. 10.1210/jcem.81.10.8855815.
103. Kogler L., Gur R.C., Derntl B. Sex differences in cognitive regulation of psychosocial achievement stress: brain and behavior. Hum. Brain Mapp. 2014, 10.1002/hbm.22683.
104. Kokras N., Dalla C., Papadopoulou-Daifoti Z. Sex differences in pharmacokinetics of antidepressants. Expert Opin. Drug Metab. Toxicol. 2011, 7(2):213-226. 10.1517/17425255.2011.544250.
105. Kudielka B.M., Kirschbaum C. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 2005, 69(1):113-132. 10.1016/j.biopsycho.2004.11.009.
106. Labad J., Menchon J.M., Alonso P., Segalas C., Jimenez S., Jaurrieta N., Vallejo J. Gender differences in obsessive-compulsive symptom dimensions. Depress. Anxiety 2008, 25(10):832-838. 10.1002/da.20332.
107. Laurent V., Westbrook R.F. Distinct contributions of the basolateral amygdala and the medial prefrontal cortex to learning and relearning extinction of context conditioned fear. Learn. Mem. 2008, 15(9):657-666. 10.1101/lm.1080108.
108. Laurent V., Westbrook R.F. Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction. Learn. Mem. 2009, 16(9):520-529. 10.1101/lm.1474609.
109. Lebron-Milad K., Milad M.R. Sex differences, gonadal hormones and the fear extinction network: implications for anxiety disorders. Biol. Mood Anxiety Disord. 2012, 2(1):3. 10.1186/2045-5380-2-3.
110. Lebron-Milad K., Abbs B., Milad M.R., Linnman C., Rougemount-Bücking A., Zeidan M.A., Goldstein J.M. Sex differences in the neurobiology of fear conditioning and extinction: a preliminary fMRI study of shared sex differences with stress-arousal circuitry. Biol. Mood Anxiety Disord. 2012, 2(1):7. 10.1186/2045-5380-2-7.
111. Lebrón-Milad K., Tsareva A., Ahmed N., Milad M.R. Sex differences and estrous cycle in female rats interact with the effects of fluoxetine treatment on fear extinction. Behav. Brain Res. 2013, 253:217-222. 10.1016/j.bbr.2013.07.024.
112. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23:155-184. 10.1146/annurev.neuro.23.1.155.
113. Leuner B., Mendolia-Loffredo S., Shors T.J. Males and females respond differently to controllability and antidepressant treatment. Biol. Psychiatry 2004, 56(12):964-970. 10.1016/j.biopsych.2004.09.018.
114. Liberzon I., Sripada C.S. The functional neuroanatomy of PTSD: a critical review. Prog. Brain Res. 2008, 167:151-169. 10.1016/S0079-6123(07)67011-3.
115. Likhtik E., Pelletier J.G., Paz R., Paré D. Prefrontal control of the amygdala. J. Neurosci. Off. J. Soc. Neurosci. 2005, 25(32):7429-7437. 10.1523/JNEUROSCI.2314-05.2005.
116. Linnman C., Rougemont-Bücking A., Beucke J.C., Zeffiro T.A., Milad M.R. Unconditioned responses and functional fear networks in human classical conditioning. Behav. Brain Res. 2011, 221(1):237-245. 10.1016/j.bbr.2011.02.045.
117. Linnman C., Zeidan M.A., Furtak S.C., Pitman R.K., Quirk G.J., Milad M.R. Resting amygdala and medial prefrontal metabolism predicts functional activation of the fear extinction circuit. Am. J. Psychiatry 2012, 169(4):415-423. 10.1176/appi.ajp.2011.10121780.
118. Lu J., Wu X.-Y., Zhu Q.-B., Li J., Shi L.-G., Wu J.-L., Bao A.-M. Sex differences in the stress response in SD rats. Behav. Brain Res. 2015, 284:231-237. 10.1016/j.bbr.2015.02.009.
119. Luine V. Sex differences in chronic stress effects on memory in rats. Stress 2002, 5(3):205-216. 10.1080/1025389021000010549.
120. Luine V., Villegas M., Martinez C., McEwen B.S. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 1994, 639(1):167-170.
121. Machado-de-Sousa J.P., Osório F.de L., Jackowski A.P., Bressan R.A., Chagas M.H.N., Torro-Alves N., DePaula A.L.D., Crippa J.A.S., Hallak J.E.C. Increased amygdalar and hippocampal volumes in young adults with social anxiety. PLoS One 2014, 9(2):e88523. 10.1371/journal.pone.0088523.
122. Maeng L.Y., Shors T.J. The stressed female brain: neuronal activity in the prelimbic but not infralimbic region of the medial prefrontal cortex suppresses learning after acute stress. Front. Neural Circ. 2013, 7:198. 10.3389/fncir.2013.00198.
123. Maeng L.Y., Waddell J., Shors T.J. The prefrontal cortex communicates with the amygdala to impair learning after acute stress in females but not in males. J. Neurosci. Off. J. Soc. Neurosci. 2010, 30(48):16188-16196. 10.1523/JNEUROSCI.2265-10.2010.
124. Maren S., De Oca B., Fanselow M.S. Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res. 1994, 661(1-2):25-34.
125. Maren S., Phan K.L., Liberzon I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 2013, 14(6):417-428. 10.1038/nrn3492.
126. Marin M.-F., Camprodon J.A., Dougherty D.D., Milad M.R. Device-based brain stimulation to augment fear extinction: implications for PTSD treatment and beyond. Depress. Anxiety 2014, 31(4):269-278. 10.1002/da.22252.
127. Maroun M. Medial prefrontal cortex: multiple roles in fear and extinction. Neuroscientist 2013, 19(4):370-383. 10.1177/1073858412464527.
128. Maroun M., Richter-Levin G. Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J. Neurosci. Off. J. Soc. Neurosci. 2003, 23(11):4406-4409.
129. McDermott C.M., Liu D., Schrader L.A. Role of gonadal hormones in anxiety and fear memory formation and inhibition in male mice. Physiol. Behav. 2012, 105(5):1168-1174. 10.1016/j.physbeh.2011.12.016.
130. McEwen B.S. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metab. Clin. Exp. 2005, 54(5 Suppl. 1):20-23. 10.1016/j.metabol.2005.01.008.
131. McEwen B.S., Weiss J.M., Schwartz L.S. Selective retention of corticosterone by limbic structures in rat brain. Nature 1968, 220(5170):911-912.
132. McGaugh J.L. Memory consolidation and the amygdala: a systems perspective. Trends Neurosci. 2002, 25(9):456.
133. McHenry J., Carrier N., Hull E., Kabbaj M. Sex differences in anxiety and depression: role of testosterone. Front. Neuroendocrinol. 2014, 35(1):42-57. 10.1016/j.yfrne.2013.09.001.
134. McLean C.P., Foa E.B. Dissemination and implementation of prolonged exposure therapy for posttraumatic stress disorder. J. Anxiety Disord. 2013, 27(8):788-792. 10.1016/j.janxdis.2013.03.004.
135. McLean C.P., Asnaani A., Litz B.T., Hofmann S.G. Gender differences in anxiety disorders: prevalence, course of illness, comorbidity and burden of illness. J. Psychiatr. Res. 2011, 45(8):1027-1035. 10.1016/j.jpsychires.2011.03.006.
136. Mennin D.S., Heimberg R.G., Turk C.L., Fresco D.M. Preliminary evidence for an emotion dysregulation model of generalized anxiety disorder. Behav. Res. Ther. 2005, 43(10):1281-1310. 10.1016/j.brat.2004.08.008.
137. Merz C.J., Tabbert K., Schweckendiek J., Klucken T., Vaitl D., Stark R., Wolf O.T. Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI. Psychoneuroendocrinology 2010, 35(1):33-46. 10.1016/j.psyneuen.2009.07.009.
138. Merz C.J., Tabbert K., Schweckendiek J., Klucken T., Vaitl D., Stark R., Wolf O.T. Neuronal correlates of extinction learning are modulated by sex hormones. Soc. Cogn. Affect. Neurosci. 2012, 7(7):819-830. 10.1093/scan/nsr063.
139. Merz C.J., Wolf O.T., Schweckendiek J., Klucken T., Vaitl D., Stark R. Stress differentially affects fear conditioning in men and women. Psychoneuroendocrinology 2013, 38(11):2529-2541. 10.1016/j.psyneuen.2013.05.015.
140. Milad M.R., Quirk G.J. Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 2012, 63:129-151. 10.1146/annurev.psych.121208.131631.
141. Milad M.R., Goldstein J.M., Orr S.P., Wedig M.M., Klibanski A., Pitman R.K., Rauch S.L. Fear conditioning and extinction: influence of sex and menstrual cycle in healthy humans. Behav. Neurosci. 2006, 120(6):1196-1203. 10.1037/0735-7044.120.5.1196.
142. Milad M.R., Wright C.I., Orr S.P., Pitman R.K., Quirk G.J., Rauch S.L. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Psychiatry 2007, 62(5):446-454. 10.1016/j.biopsych.2006.10.011.
143. Milad M.R., Igoe S.A., Lebron-Milad K., Novales J.E. Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience 2009, 164(3):887-895. 10.1016/j.neuroscience.2009.09.011.
144. Milad M.R., Pitman R.K., Ellis C.B., Gold A.L., Shin L.M., Lasko N.B., Rauch S.L. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol. Psychiatry 2009, 66(12):1075-1082. 10.1016/j.biopsych.2009.06.026.
145. Milad M.R., Zeidan M.A., Contero A., Pitman R.K., Klibanski A., Rauch S.L., Goldstein J.M. The influence of gonadal hormones on conditioned fear extinction in healthy humans. Neuroscience 2010, 168(3):652-658. 10.1016/j.neuroscience.2010.04.030.
146. Milad M.R., Furtak S.C., Greenberg J.L., Keshaviah A., Im J.J., Falkenstein M.J., Wilhelm S. Deficits in conditioned fear extinction in obsessive-compulsive disorder and neurobiological changes in the fear circuit. JAMA Psychiatry 2013, 70(6):608-618. (quiz 554). 10.1001/jamapsychiatry.2013.914.
147. Mitra R., Sapolsky R.M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. 2008, 105(14):5573-5578. 10.1073/pnas.0705615105.
148. Mitra R., Jadhav S., McEwen B.S., Vyas A., Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(26):9371-9376. 10.1073/pnas.0504011102.
149. Möller A.T., Bäckström T., Nyberg S., Söndergaard H.P., Helström L. Women with PTSD have a changed sensitivity to GABA-A receptor active substances. Psychopharmacology 2014, 10.1007/s00213-014-3776-y.
150. Morgan M.A., Pfaff D.W. Effects of estrogen on activity and fear-related behaviors in mice. Horm. Behav. 2001, 40(4):472-482. 10.1006/hbeh.2001.1716.
151. Nielsen S.E., Ertman N., Lakhani Y.S., Cahill L. Hormonal contraception usage is associated with altered memory for an emotional story. Neurobiol. Learn. Mem. 2011, 96(2):378-384. 10.1016/j.nlm.2011.06.013.
152. Nielsen S.E., Segal S.K., Worden I.V., Yim I.S., Cahill L. Hormonal contraception use alters stress responses and emotional memory. Biol. Psychol. 2013, 92(2):257-266. 10.1016/j.biopsycho.2012.10.007.
153. Nielsen S.E., Ahmed I., Cahill L. Postlearning stress differentially affects memory for emotional gist and detail in naturally cycling women and women on hormonal contraceptives. Behav. Neurosci. 2014, 128(4):482-493. 10.1037/a0036687.
154. Nillni Y.I., Toufexis D.J., Rohan K.J. Anxiety sensitivity, the menstrual cycle, and panic disorder: a putative neuroendocrine and psychological interaction. Clin. Psychol. Rev. 2011, 31(7):1183-1191. 10.1016/j.cpr.2011.07.006.
155. Nolen-Hoeksema S. Responses to depression and their effects on the duration of depressive episodes. J. Abnorm. Psychol. 1991, 100(4):569-582.
156. Nolen-Hoeksema S., Girgus J.S. The emergence of gender differences in depression during adolescence. Psychol. Bull. 1994, 115(3):424-443.
157. Norrholm S.D., Jovanovic T., Olin I.W., Sands L.A., Karapanou I., Bradley B., Ressler K.J. Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity. Biol. Psychiatry 2011, 69(6):556-563. 10.1016/j.biopsych.2010.09.013.
158. Pace-Schott E.F., Spencer R.M.C., Vijayakumar S., Ahmed N.A.K., Verga P.W., Orr S.P., Milad M.R. Extinction of conditioned fear is better learned and recalled in the morning than in the evening. J. Psychiatr. Res. 2013, 47(11):1776-1784. 10.1016/j.jpsychires.2013.07.027.
159. Patel P.D., Katz M., Karssen A.M., Lyons D.M. Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex. Psychoneuroendocrinology 2008, 33(3):360-367. 10.1016/j.psyneuen.2007.12.003.
160. Perrin M., Vandeleur C.L., Castelao E., Rothen S., Glaus J., Vollenweider P., Preisig M. Determinants of the development of post-traumatic stress disorder, in the general population. Soc. Psychiatry Psychiatr. Epidemiol. 2014, 49(3):447-457. 10.1007/s00127-013-0762-3.
161. Phelps E.A., Delgado M.R., Nearing K.I., LeDoux J.E. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 2004, 43(6):897-905. 10.1016/j.neuron.2004.08.042.
162. 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(14):5567-5572. 10.1073/pnas.0801853105.
163. Piccinelli M., Wilkinson G. Gender differences in depression. Critical review. Br. J. Psychiatry J. Ment. Sci. 2000, 177:486-492.
164. Pigott T.A. Anxiety disorders in women. Psychiatr. Clin. N. Am. 2003, 26(3):621-672. (vi-vii).
165. Pinna G., Rasmusson A.M. Ganaxolone improves behavioral deficits in a mouse model of post-traumatic stress disorder. Front. Cell. Neurosci. 2014, 8:256. 10.3389/fncel.2014.00256.
166. Pitman R.K., Rasmusson A.M., Koenen K.C., Shin L.M., Orr S.P., Gilbertson M.W., Liberzon I. Biological studies of post-traumatic stress disorder. Nat. Rev. Neurosci. 2012, 13(11):769-787. 10.1038/nrn3339.
167. Pope H.G., Cohane G.H., Kanayama G., Siegel A.J., Hudson J.I. Testosterone gel supplementation for men with refractory depression: a randomized, placebo-controlled trial. Am. J. Psychiatry 2003, 160(1):105-111.
168. Protopopescu X., Pan H., Altemus M., Tuescher O., Polanecsky M., McEwen B., Stern E. Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(44):16060-16065. 10.1073/pnas.0502818102.
169. Pryce C.R., Lehmann J., Feldon J. Effect of sex on fear conditioning is similar for context and discrete CS in Wistar, Lewis and Fischer rat strains. Pharmacol. Biochem. Behav. 1999, 64(4):753-759.
170. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33(1):56-72. 10.1038/sj.npp.1301555.
171. Quirk G.J., Russo G.K., Barron J.L., Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J. Neurosci. Off. J. Soc. Neurosci. 2000, 20(16):6225-6231.
172. Quirk G.J., Likhtik E., Pelletier J.G., Paré D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J. Neurosci. Off. J. Soc. Neurosci. 2003, 23(25):8800-8807.
173. Rasmusson A.M., Pinna G., Paliwal P., Weisman D., Gottschalk C., Charney D., Guidotti A. Decreased cerebrospinal fluid allopregnanolone levels in women with posttraumatic stress disorder. Biol. Psychiatry 2006, 60(7):704-713. 10.1016/j.biopsych.2006.03.026.
174. Reed V., Wittchen H.U. DSM-IV panic attacks and panic disorder in a community sample of adolescents and young adults: how specific are panic attacks?. J. Psychiatr. Res. 1998, 32(6):335-345.
175. Ressler K.J., Mercer K.B., Bradley B., Jovanovic T., Mahan A., Kerley K., May V. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 2011, 470(7335):492-497. 10.1038/nature09856.
176. Rey C.D., Lipps J., Shansky R.M. Dopamine D1 receptor activation rescues extinction impairments in low-estrogen female rats and induces cortical layer-specific activation changes in prefrontal-amygdala circuits. Neuropsychopharmacology 2014, 39(5):1282-1289. 10.1038/npp.2013.338.
177. Ribeiro A.M., Barbosa F.F., Godinho M.R., Fernandes V.S., Munguba H., Melo T.G., Silva R.H. Sex differences in aversive memory in rats: possible role of extinction and reactive emotional factors. Brain Cogn. 2010, 74(2):145-151. 10.1016/j.bandc.2010.07.012.
178. Rivas-Arancibia S., Vazquez-Pereyra F. Hormonal modulation of extinction responses induced by sexual steroid hormones in rats. Life Sci. 1994, 54(21):L363-L367.
179. Ross L.E., McLean L.M. Anxiety disorders during pregnancy and the postpartum period: a systematic review. J. Clin. Psychiatry 2006, 67(8):1285-1298.
180. Seedat S., Stein D.J., Carey P.D. Post-traumatic stress disorder in women: epidemiological and treatment issues. CNS Drugs 2005, 19(5):411-427.
181. Shansky R.M., Lipps J. Stress-induced cognitive dysfunction: hormone-neurotransmitter interactions in the prefrontal cortex. Front. Hum. Neurosci. 2013, 7. 10.3389/fnhum.2013.00123.
182. Shansky R.M., Morrison J.H. Stress-induced dendritic remodeling in the medial prefrontal cortex: effects of circuit, hormones and rest. Brain Res. 2009, 1293:108-113. 10.1016/j.brainres.2009.03.062.
183. Shansky R.M., Hamo C., Hof P.R., Lou W., McEwen B.S., Morrison J.H. Estrogen promotes stress sensitivity in a prefrontal cortex-amygdala pathway. Cereb. Cortex 2010, 20(11):2560-2567. 10.1093/cercor/bhq003.
184. Shin L.M., Rauch S.L., Pitman R.K. Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann. N. Y. Acad. Sci. 2006, 1071:67-79. 10.1196/annals.1364.007.
185. Shores M.M., Sloan K.L., Matsumoto A.M., Moceri V.M., Felker B., Kivlahan D.R. Increased incidence of diagnosed depressive illness in hypogonadal older men. Arch. Gen. Psychiatry 2004, 61(2):162-167. 10.1001/archpsyc.61.2.162.
186. Shors T.J., Leuner B. Estrogen-mediated effects on depression and memory formation in females. J. Affect. Disord. 2003, 74(1):85.
187. Shors T.J., Lewczyk C., Pacynski M., Mathew P.R., Pickett J. Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 1998, 9(3):419-423.
188. Shughrue P.J., Scrimo P.J., Merchenthaler I. Evidence for the colocalization of estrogen receptor-beta mRNA and estrogen receptor-alpha immunoreactivity in neurons of the rat forebrain. Endocrinology 1998, 139(12):5267-5270. 10.1210/endo.139.12.6525.
189. Shvil E., Sullivan G.M., Schafer S., Markowitz J.C., Campeas M., Wager T.D., Neria Y. Sex differences in extinction recall in posttraumatic stress disorder: a pilot fMRI study. Neurobiol. Learn. Mem. 2014, 113:101-108. 10.1016/j.nlm.2014.02.003.
190. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 2011, 36(2):529-538. 10.1038/npp.2010.184.
191. Silberg J., Pickles A., Rutter M., Hewitt J., Simonoff E., Maes H., Eaves L. The influence of genetic factors and life stress on depression among adolescent girls. Arch. Gen. Psychiatry 1999, 56(3):225-232.
192. Sonnenberg C.M., Beekman A.T., Deeg D.J., van Tilburg W. Sex differences in late-life depression. Acta Psychiatr. Scand. 2000, 101(4):286-292.
193. Sotres-Bayon F., Bush D.E.A., LeDoux J.E. Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn. Mem. 2004, 11(5):525-535. 10.1101/lm.79504.
194. Sotres-Bayon F., Sierra-Mercado D., Pardilla-Delgado E., Quirk G.J. Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 2012, 76(4):804-812. 10.1016/j.neuron.2012.09.028.
195. Sripada R.K., Marx C.E., King A.P., Rampton J.C., Ho S.S., Liberzon I. Allopregnanolone elevations following pregnenolone administration are associated with enhanced activation of emotion regulation neurocircuits. Biol. Psychiatry 2013, 73(11):1045-1053. 10.1016/j.biopsych.2012.12.008.
196. Sripada R.K., Welsh R.C., Marx C.E., Liberzon I. The neurosteroids allopregnanolone and dehydroepiandrosterone modulate resting-state amygdala connectivity. Hum. Brain Mapp. 2014, 35(7):3249-3261. 10.1002/hbm.22399.
197. Stark R., Wolf O.T., Tabbert K., Kagerer S., Zimmermann M., Kirsch P., Vaitl D. Influence of the stress hormone cortisol on fear conditioning in humans: evidence for sex differences in the response of the prefrontal cortex. NeuroImage 2006, 32(3):1290-1298. 10.1016/j.neuroimage.2006.05.046.
198. Ter Horst G.J., Wichmann R., Gerrits M., Westenbroek C., Lin Y. Sex differences in stress responses: focus on ovarian hormones. Physiol. Behav. 2009, 97(2):239-249. 10.1016/j.physbeh.2009.02.036.
199. Ter Horst J.P., Carobrez A.P., van der Mark M.H., de Kloet E.R., Oitzl M.S. Sex differences in fear memory and extinction of mice with forebrain-specific disruption of the mineralocorticoid receptor. Eur. J. Neurosci. 2012, 36(8):3096-3102. 10.1111/j.1460-9568.2012.08237.x.
200. Tolin D.F., Foa E.B. Sex differences in trauma and posttraumatic stress disorder: a quantitative review of 25years of research. Psychol. Bull. 2006, 132(6):959-992. 10.1037/0033-2909.132.6.959.
201. Toufexis D.J., Davis C., Hammond A., Davis M. Progesterone attenuates corticotropin-releasing factor-enhanced but not fear-potentiated startle via the activity of its neuroactive metabolite, allopregnanolone. J. Neurosci. Off. J. Soc. Neurosci. 2004, 24(45):10280-10287. 10.1523/JNEUROSCI.1386-04.2004.
202. Toufexis D., Rivarola M.A., Lara H., Viau V. Stress and the reproductive axis. J. Neuroendocrinol. 2014, 26(9):573-586. 10.1111/jne.12179.
203. Van der Veen D.C., van Zelst W.H., Schoevers R.A., Comijs H.C., Voshaar R.C.O. Comorbid anxiety disorders in late-life depression: results of a cohort study. Int. Psychogeriatr. 2014, 1-9. 10.1017/S1041610214002312.
204. Van Veen J.F., Jonker B.W., van Vliet I.M., Zitman F.G. The effects of female reproductive hormones in generalized social anxiety disorder. Int. J. Psychiatry Med. 2009, 39(3):283-295.
205. Veldhuis H.D., Van Koppen C., Van Ittersum M., De Kloet E.R. Specificity of the adrenal steroid receptor system in rat hippocampus. Endocrinology 1982, 110(6):2044-2051. 10.1210/endo-110-6-2044.
206. Vesga-López O., Blanco C., Keyes K., Olfson M., Grant B.F., Hasin D.S. Psychiatric disorders in pregnant and postpartum women in the United States. Arch. Gen. Psychiatry 2008, 65(7):805-815. 10.1001/archpsyc.65.7.805.
207. Wang C., Alexander G., Berman N., Salehian B., Davidson T., McDonald V., Swerdloff R.S. Testosterone replacement therapy improves mood in hypogonadal men-a clinical research center study. J. Clin. Endocrinol. Metab. 1996, 81(10):3578-3583. 10.1210/jcem.81.10.8855804.
208. Watanabe Y., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 1992, 588(2):341-345.
209. Wegerer M., Kerschbaum H., Blechert J., Wilhelm F.H. Low levels of estradiol are associated with elevated conditioned responding during fear extinction and with intrusive memories in daily life. Neurobiol. Learn. Mem. 2014, 116:145-154. 10.1016/j.nlm.2014.10.001.
210. Weinberg M.S., Johnson D.C., Bhatt A.P., Spencer R.L. Medial prefrontal cortex activity can disrupt the expression of stress response habituation. Neuroscience 2010, 168(3):744-756. 10.1016/j.neuroscience.2010.04.006.
211. Wellman C.L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J. Neurobiol. 2001, 49(3):245-253.
212. Wood G.E., Shors T.J. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(7):4066-4071.
213. Yuan D.L., Chambers K.C. Estradiol accelerates extinction of a conditioned taste aversion in female and male rats. Horm. Behav. 1999, 36(1):1-16. 10.1006/hbeh.1999.1520.
214. Zarrouf F.A., Artz S., Griffith J., Sirbu C., Kommor M. Testosterone and depression: systematic review and meta-analysis. J. Psychiatr. Pract. 2009, 15(4):289-305. 10.1097/01.pra.0000358315.88931.fc.
215. Zeidan M.A., Igoe S.A., Linnman C., Vitalo A., Levine J.B., Klibanski A., Milad M.R. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol. Psychiatry 2011, 70(10):920-927. 10.1016/j.biopsych.2011.05.016.
216. Zorawski M., Cook C.A., Kuhn C.M., LaBar K.S. Sex, stress, and fear: individual differences in conditioned learning. Cogn. Affect. Behav. Neurosci. 2005, 5(2):191-201.
217. Zorawski M., Blanding N.Q., Kuhn C.M., LaBar K.S. Effects of stress and sex on acquisition and consolidation of human fear conditioning. Learn. Mem. 2006, 13(4):441-450. 10.1101/lm.189106.