Enduring influence of pubertal stressors on behavioral response to hormones in female mice

Hormones and Behavior

Volumn 64, Issue 2, 2013, Pages 390-398

  Blaustein, Jeffrey D ^a   Ismail, Nafissa ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Anxiety; Cognitive function; Depression; Estradiol; Immune challenge; Lipopolysaccharide; Progesterone; Puberty; Sexual behavior; Stress

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; PROGESTERONE;

ANIMAL BEHAVIOR; DEVELOPMENTAL STAGE; FEMALE; HORMONE RELEASE; HORMONE RESPONSE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PUBERTY; REVIEW; SEX DIFFERENTIATION; STRESS;

ANXIETY; COGNITIVE FUNCTION; DEPRESSION; ESTRADIOL; IMMUNE CHALLENGE; LIPOPOLYSACCHARIDE; PROGESTERONE; PUBERTY; SEXUAL BEHAVIOR; STRESS;

ANIMALS; BEHAVIOR, ANIMAL; CORTICOSTERONE; FEMALE; GONADAL HORMONES; IMMUNITY; MICE; SEXUAL MATURATION; STRESS, PSYCHOLOGICAL;

EID: 84883565436     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.01.015     Document Type: Review

References (112)

1. Amin Z., Canli T., Epperson C.N. Effect of estrogen-serotonin interactions on mood and cognition. Behav. Cogn. Neurosci. Rev. 2005, 4:43-58.
2. Andersen S.L. Trajectories of brain development: point of vulnerability or window of opportunity?. Neurosci. Biobehav. Rev. 2003, 27:3-18.
3. Angold A., Costello E.J. Puberty and depression. Child Adolesc. Psychiatr. Clin. N. Am. 2006, 15:919-937. (ix).
4. Anisman H. Cascading effects of stressors and inflammatory immune system activation: implications for major depressive disorder. J. Psychiatry Neurosci. 2009, 34:4-20.
5. Avital A., Richter-Levin G. Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int. J. Neuropsychopharmacol. 2005, 8:163-173.
6. Bekku N., Yoshimura H. Animal model of menopausal depressive-like state in female mice: prolongation of immobility time in the forced swimming test following ovariectomy. Psychopharmacology (Berl.) 2005, 183:300-307.
7. Bernardi M., Vergoni A.V., Sandrini M., Tagliavini S., Bertolini A. Influence of ovariectomy, estradiol and progesterone on the behavior of mice in an experimental model of depression. Physiol. Behav. 1989, 45:1067-1068.
8. Bertone-Johnson E.R., Whitcomb B.W., Missmer S.A., Karlson E.W., Rich-Edwards J.W. Inflammation and early-life abuse in women. Am. J. Prev. Med. 2012, 43:611-620.
9. Blaustein J.D. Feminine reproductive behavior and physiology in rodents: integration of hormonal, behavioral and environmental influences. Hormones, Brain and Behavior 2009, 67-107. Elsevier, Philadelphia. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
10. Bloch M., Schmidt P.J., Danaceau M., Murphy J., Nieman L., Rubinow D.R. Effects of gonadal steroids in women with a history of postpartum depression. Am. J. Psychiatry 2000, 157:924-930.
11. Bloch M., Daly R.C., Rubinow D.R. Endocrine factors in the etiology of postpartum depression. Compr. Psychiatry 2003, 44:234-246.
12. Choleris E., Gustafsson J.A., Korach K.S., Muglia L.J., Pfaff D.W., Ogawa S. An estrogen-dependent four-gene micronet regulating social recognition: A study with oxytocin and estrogen receptor- alpha and -beta knockout mice. Proc. Natl. Acad. Sci. U. S. A 2003, 100:6192-6197.
13. Choleris E., Ogawa S., Kavaliers M., Gustafsson J.A., Korach K.S., Muglia L.J., Pfaff D.W. Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: A detailed behavioral analysis with knockout female mice. Genes Brain Behav. 2006, 5:528-539.
14. Conrad K.L., Winder D.G. Altered anxiety-like behavior and long-term potentiation in the bed nucleus of the stria terminalis in adult mice exposed to chronic social isolation, unpredictable stress, and ethanol beginning in adolescence. Alcohol 2011, 45:585-593.
15. Costello E.J., Mustillo S., Erkanli A., Keeler G., Angold A. Prevalence and development of psychiatric disorders in childhood and adolescence. Arch. Gen. Psychiatry 2003, 60:837-844.
16. Dalla C., Antoniou K., Papadopoulou-Daifoti Z., Balthazart J., Bakker J. Oestrogen-deficient female aromatase knockout (ArKO) mice exhibit depressive-like symptomatology. Eur. J. Neurosci. 2004, 20:217-228.
17. Danese A., McEwen B.S. Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiol. Behav. 2012, 106:29-39.
18. Danese A., Pariante C.M., Caspi A., Taylor A., Poulton R. Childhood maltreatment predicts adult inflammation in a life-course study. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1319-1324.
19. Danese A., Moffitt T.E., Pariante C.M., Ambler A., Poulton R., Caspi A. Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Arch. Gen. Psychiatry 2008, 65:409-415.
20. Danese A., Moffitt T.E., Harrington H., Milne B.J., Polanczyk G., Pariante C.M., Poulton R., Caspi A. Adverse childhood experiences and adult risk factors for age-related disease: depression, inflammation, and clustering of metabolic risk markers. Arch. Pediatr. Adolesc. Med. 2009, 163:1135-1143.
21. Danese A., Caspi A., Williams B., Ambler A., Sugden K., Mika J., Werts H., Freeman J., Pariante C.M., Moffitt T.E., Arseneault L. Biological embedding of stress through inflammation processes in childhood. Mol. Psychiatry 2011, 16:244-246.
22. Dantzer R. Cytokine-induced sickness behavior: mechanisms and implications. Ann. N.Y. Acad. Sci. 2001, 933:222-234.
23. de Kloet E.R., Sibug R.M., Helmerhorst F.M., Schmidt M.V. Stress, genes and the mechanism of programming the brain for later life. Neurosci. Biobehav. Rev. 2005, 29:271-281.
24. DeCatanzaro D., Knipping R.P., Gorzalka B.B. Antagonism of estrogen-induced lordosis by corticosterone in adrenalectomized-ovariectomized female rats and mice. Pharmacol. Biochem. Behav. 1981, 15:761-766.
25. Diaz-Veliz G., Soto V., Dussaubat N., Mora S. Influence of the estrous cycle, ovariectomy and estradiol replacement upon the acquisition of conditioned avoidance responses in rats. Physiol. Behav. 1989, 46:397-401.
26. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors. Physiol. Behav. 1991, 50:61-65.
27. Diaz-Veliz G., Alarcon T., Espinoza C., Dussaubat N., Mora S. Ketanserin and anxiety levels: influence of gender, estrous cycle, ovariectomy and ovarian hormones in female rats. Pharmacol. Biochem. Behav. 1997, 58:637-642.
28. Estrada-Camarena E., Lopez-Rubalcava C., Fernandez-Guasti A. Facilitating antidepressant-like actions of estrogens are mediated by 5-HT1A and estrogen receptors in the rat forced swimming test. Psychoneuroendocrinology 2006, 31:905-914.
29. Galea L.A.N., Wide J.K., Barr A.M. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav. Brain Res. 2001, 122:1-9.
30. Ge X., Conger R.D., Elder G.H. Pubertal transition, stressful life events, and the emergence of gender differences in adolescent depressive symptoms. Dev. Psychol. 2001, 37:404-417.
31. Gilpin N.W., Karanikas C.A., Richardson H.N. Adolescent binge drinking leads to changes in alcohol drinking, anxiety, and amygdalar corticotropin releasing factor cells in adulthood in male rats. PLoS One 2012, 7:e31466.
32. Harsh V., Meltzer-Brody S., Rubinow D.R., Schmidt P.J. Reproductive aging, sex steroids, and mood disorders. Harv. Rev. Psychiatry 2009, 17:87-102.
33. Hayward C., Sanborn K. Puberty and the emergence of gender differences in psychopathology. J. Adolesc. Health 2002, 30:49-58.
34. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 2001, 49:1023-1039.
35. Heim C., Plotsky P.M., Nemeroff C.B. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 2004, 29:641-648.
36. Hodes G.E., Shors T.J. Distinctive stress effects on learning during puberty. Horm. Behav. 2005, 48:163-171.
37. Imwalle D.B., Gustafsson J.A., Rissman E.F. Lack of functional estrogen receptor beta influences anxiety behavior and serotonin content in female mice. Physiol. Behav. 2005, 84:157-163.
38. Isgor C., Kabbaj M., Akil H., Watson S.J. Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 2004, 14:636-648.
39. Ismail, N., Blaustein, J.D., in press. Pubertal immune challenge blocks the ability of estradiol to enhance performance on cognitive tasks in adult female mice. Psychoneuroendocrinology, (S0306-4530(12)00359-9 [pii]). http://dx.doi.org/10.1016/j.psyneuen.2012.11.003.
40. Ismail N., Garas P., Blaustein J.D. Long-term effects of pubertal stressors on female sexual receptivity and estrogen receptor-alpha expression in CD-1 female mice. Horm. Behav. 2011, 59:565-571.
41. Ismail, N., Kumlin, A.M., Blaustein, J.D., in press. A pubertal immune challenge alters the antidepressant-like effects of chronic estradiol treatment in inbred and outbred adult female mice. Neuroscience, (S0306-4522(12)00967-0 [pii]). http://dx.doi.org/10.1016/j.neuroscience.2012.09.047.
42. Kabbaj M., Isgor C., Watson S.J., Akil H. Stress during adolescence alters behavioral sensitization to amphetamine. Neuroscience 2002, 113:395-400.
43. Kaiser S., Kruijver F.P.M., Straub R.H., Sachser N., Swaab D.F. Early social stress in male guinea-pigs changes social behaviour, and autonomic and neuroendocrine functions. J. Neuroendocrinol. 2003, 15:761-769.
44. Koss W.A., Einat H., Schloesser R.J., Manji H.K., Rubinow D.R. Estrogen effects on the forced swim test differ in two outbred rat strains. Physiol. Behav. 2012, 106:81-86.
45. Krezel W., Dupont S., Krust A., Chambon P., Chapman P.F. Increased anxiety and synaptic plasticity in estrogen receptor beta- deficient mice. Proc. Natl. Acad. Sci. U. S. A 2001, 98:12278-12282.
46. Lagunas N., Calmarza-Font I., Diz-Chaves Y., Garcia-Segura L.M. Long-term ovariectomy enhances anxiety and depressive-like behaviors in mice submitted to chronic unpredictable stress. Horm. Behav. 2010, 58:786-791.
47. Laroche, J., 2008. Neuroendocrine effects of pubertal stress exposure in the female mouse. Dissertation, University of Massachusetts. United States - Massachusetts: Dissertations & Theses @ University of Massachusetts @ Amherst; ProQuest Dissertations & Theses A&I.
48. Laroche J., Gasbarro L., Herman J.P., Blaustein J.D. Enduring influences of peripubertal/adolescent stressors on behavioral response to estradiol and progesterone in adult female mice. Endocrinology 2009, 150:3717-3725.
49. Laroche J., Gasbarro L., Herman J.P., Blaustein J.D. Reduced behavioral response to gonadal hormones in mice shipped during the peripubertal/adolescent period. Endocrinology 2009, 150:2351-2358.
50. Laugero K.D., Moberg G.P. Summation of behavioral and immunological stress: metabolic consequences to the growing mouse. Am. J. Physiol. Endocrinol. Metab. 2000, 279:E44-E49.
51. Lemieux A., Coe C.L., Carnes M. Symptom severity predicts degree of T cell activation in adult women following childhood maltreatment. Brain Behav. Immun. 2008, 22:994-1003.
52. Li X., Morrow D., Witkin J.M. Decreases in nestlet shredding of mice by serotonin uptake inhibitors: comparison with marble burying. Life Sci. 2006, 78:1933-1939.
53. Luine V.N. Sex steroids and cognitive function. J. Neuroendocrinol. 2008, 20:866-872.
54. McCormick C.M., Mathews I.Z. HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol. Biochem. Behav. 2007, 86:220-233.
55. McCormick C.M., Robarts D., Gleason E., Kelsey J.E. Stress during adolescence enhances locomotor sensitization to nicotine in adulthood in female, but not male, rats. Horm. Behav. 2004, 46:458-466.
56. McCormick C.M., Robarts D., Kopeikina K., Kelsey J.E. Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm. Behav. 2005, 48:64-74.
57. McCormick C.M., Mathews I.Z., Thomas C., Waters P. Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn. 2010, 72:73-85.
58. Meaney M.J., Aitken D.H. The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Brain Res. 1985, 354:301-304.
59. Meaney M.J., Aitken D.H., Bodnoff S.R., Iny L.J., Tatarewicz J.E., Sapolsky R.M. Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behav. Neurosci. 1985, 99:765-770.
60. Meaney M.J., Sapolsky R.M., McEwen B.S. The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Dev. Brain Res. 1985, 18:159-164.
61. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65:732-741.
62. Mora S., Dussaubat N., Diaz-Veliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996, 21:609-620.
63. Morgan M.A., Pfaff D.W. Effects of estrogen on activity and fear-related behaviors in mice. Horm. Behav. 2001, 40:472-482.
64. Morgan M.A., Pfaff D.W. Estrogen's effects on activity, anxiety, and fear in two mouse strains. Behav. Brain Res. 2002, 132:85-93.
65. Musatov S., Chen W., Pfaff D.W., Kaplitt M.G., Ogawa S. RNAi-mediated silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10456-10460.
66. Ogawa S., Eng V., Taylor J., Lubahn D.B., Korach K.S., Pfaff D.W. Roles of estrogen receptor alpha gene expression in reproduction- related behaviors in female mice. Endocrinology 1998, 139:5070-5081.
67. Ojeda S.R., Weaton J.E., Jameson H.E., McCann S.M. The onset of puberty in the female rat: changes in plasma prolactin, gonadotropins, luteinizing hormone-releasing hormone (LHRH), and hypothalamic LHRH content. Endocrinology 1976, 98:630-638.
68. Okada M., Hayashi N., Kometani M., Nakao K., Inukai T. Influences of ovariectomy and continuous replacement of 17beta-estradiol on the tail skin temperature and behavior in the forced swimming test in rats. Jpn. J. Pharmacol. 1997, 73:93-96.
69. Olesen K.M., Ismail N., Merchasin E.D., Blaustein J.D. Long-term alteration of anxiolytic effects of ovarian hormones in female mice by a peripubertal immune challenge. Horm. Behav. 2011, 60:318-326.
70. Olivera-Lopez J.I., Molina-Hernandez M., Tellez-Alcantara N.P., Jaramillo M.T. Estradiol and neuropeptide Y (intra-lateral septal) reduce anxiety-like behavior in two animal models of anxiety. Peptides 2008, 29:1396-1403.
71. Osterlund M.K., Witt M.R., Gustafsson J.A. Estrogen action in mood and neurodegenerative disorders: estrogenic compounds with selective properties-the next generation of therapeutics. Endocrine 2005, 28:235-242.
72. Pace T.W., Wingenfeld K., Schmidt I., Meinlschmidt G., Hellhammer D.H., Heim C.M. Increased peripheral NF-kappaB pathway activity in women with childhood abuse-related posttraumatic stress disorder. Brain Behav. Immun. 2012, 26:13-17.
73. Pandaranandaka J., Poonyachoti S., Kalandakanond-Thongsong S. Anxiolytic property of estrogen related to the changes of the monoamine levels in various brain regions of ovariectomized rats. Physiol. Behav. 2006, 87:828-835.
74. Pandaranandaka J., Poonyachoti S., Kalandakanond-Thongsong S. Differential effects of exogenous and endogenous estrogen on anxiety as measured by elevated T-maze in relation to the serotonergic system. Behav. Brain Res. 2009, 198:142-148.
75. Parker C.R., Mahesh V.B. Hormonal events surrounding the natural onset of puberty in female rats. Biol. Reprod. 1976, 14:347-353.
76. Paus T., Keshavan M., Giedd J.N. Why do many psychiatric disorders emerge during adolescence?. Nat. Rev. Neurosci. 2008, 9:947-957.
77. Payne J.L. The role of estrogen in mood disorders in women. Int. Rev. Psychiatry 2003, 15:280-290.
78. Picazo O., Estrada-Camarena E., Hernandez-Aragon A. Influence of the post-ovariectomy time frame on the experimental anxiety and the behavioural actions of some anxiolytic agents. Eur. J. Pharmacol. 2006, 530:88-94.
79. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 1977, 229:327-336.
80. Rachman I.M., Unnerstall J.R., Pfaff D.W., Cohen R.S. Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13941-13946.
81. Raison C.L., Miller A.H. Is depression an inflammatory disorder?. Curr. Psychiatry Rep. 2011, 13:467-475.
82. Rissman E.F., Wersinger S.R., Fugger H.N., Foster T.C. Sex with knockout models: behavioral studies of estrogen receptor alpha. Brain Res. 1999, 835:80-90.
83. Rivest S. Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 2009, 9:429-439.
84. Rocca W.A., Grossardt B.R., Geda Y.E., Gostout B.S., Bower J.H., de Maraganore D.M., Melton L.J. Long-term risk of depressive and anxiety symptoms after early bilateral oophorectomy. Menopause 2008, 15:1050-1059.
85. Romeo R.D. Adolescence: a central event in shaping stress reactivity. Dev. Psychobiol. 2010, 52:244-253.
86. Romeo R.D., Mueller A., Sisti H.M., Ogawa S., McEwen B.S., Brake W.G. Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Horm. Behav. 2003, 43:561-567.
87. Romeo R.D., Lee S.J., Chhua N., McPherson C.R., McEwen B.S. Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 2004, 79:125-132.
88. Romeo R.D., Bellani R., Karatsoreos I.N., Chhua N., Vernov M., Conrad C.D., McEwen B.S. Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology 2006, 147:1664-1674.
89. Rubinow D.R., Schmidt P.J. The treatment of premenstrual syndrome - forward into the past. N. Engl. J. Med. 1995, 332(23):1574-1575. (JUN 8).
90. Sanchez M.M., Ladd C.O., Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 2001, 13:419-449.
91. Schmidt P.J. Depression, the perimenopause, and estrogen therapy. Ann. N. Y. Acad. Sci. 2005, 1052:27-40.
92. Schmidt P.J., Nieman L., Danaceau M.A., Tobin M.B., Roca C.A., Murphy J.H., Rubinow D.R. Estrogen replacement in perimenopause-related depression: a preliminary report. Am. J. Obstet. Gynecol. 2000, 183:414-420.
93. Shea A., Walsh C., Macmillan H., Steiner M. Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 2005, 30:162-178.
94. Sisk C.L., Foster D.L. The neural basis of puberty and adolescence. Nat. Neurosci. 2004, 7:1040-1047.
95. Sisk C.L., Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 2005, 26:163-174.
96. Sizonenko P.C. Physiology of puberty. J. Endocrinol. Invest. 1989, 12:59-63.
97. Soucy G., Boivin G., Labrie F., Rivest S. Estradiol is required for a proper immune response to bacterial and viral pathogens in the female brain. J. Immunol. 2005, 174:6391-6398.
98. Spencer S.J., Boisse L., Mouihate A., Pittman Q.J. Long term alterations in neuroimmune responses of female rats after neonatal exposure to lipopolysaccharide. Brain Behav. Immun. 2006, 20:325-330.
99. Spencer S.J., Martin S., Mouihate A., Pittman Q.J. Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge. Neuropsychopharmacology 2006, 31:1910-1918.
100. Spencer S.J., Field E., Pittman Q.J. Neonatal programming by neuroimmune challenge: effects on responses and tolerance to septic doses of lipopolysaccharide in adult male and female rats. J. Neuroendocrinol. 2010, 22:272-281.
101. Stoffel E.C., Craft R.M. Ovarian hormone withdrawal-induced "depression" in female rats. Physiol. Behav. 2004, 83:505-513.
102. Suda S., Segi-Nishida E., Newton S.S., Duman R.S. A postpartum model in rat: behavioral and gene expression changes induced by ovarian steroid deprivation. Biol. Psychiatry 2008, 64:311-319.
103. Tarullo A.R., Gunnar M.R. Child maltreatment and the developing HPA axis. Horm. Behav. 2006, 50:632-639.
104. Teicher M.H., Andersen S.L., Polcari A., Anderson C.M., Navalta C.P., Kim D.M. The neurobiological consequences of early stress and childhood maltreatment. Neurosci. Biobehav. Rev. 2003, 27:33-44.
105. Toledo-Rodriguez M., Sandi C. Stress during adolescence increases novelty seeking and risk-taking behavior in male and female rats. Front. Behav. Neurosci. 2011, 5:17.
106. Tomihara K., Soga T., Nomura M., Korach K.S., Gustafsson J.A., Pfaff D.W., Ogawa S. Effect of ER-beta gene disruption on estrogenic regulation of anxiety in female mice. Physiol. Behav. 2009, 96:300-306.
107. Vandenbergh J.G. Effect of the presence of a male on the sexual maturation of female mice. Endocrinology 1967, 81:345-349.
108. Vandenbergh J.G. Male odor accelerates female sexual maturation in mice. Endocrinology 1969, 84:658-660.
109. Wang H., Meng X.H., Ning H., Zhao X.F., Wang Q., Liu P., Zhang H., Zhang C., Chen G.H., Xu D.X. Age- and gender-dependent impairments of neurobehaviors in mice whose mothers were exposed to lipopolysaccharide during pregnancy. Toxicol. Lett. 2010, 192:245-251.
110. Ward I.L. The prenatal stress syndrome: current status. Psychoneuroendocrinology 1984, 9:3-11.
111. Waylen A., Wolke D. Sex 'n' drugs 'n' rock 'n' roll: the meaning and social consequences of pubertal timing. Eur. J. Endocrinol. 2004, 151(Suppl. 3):U151-U159.
112. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 2008, 32:1073-1086.