Neonatal testosterone partially organizes sex differences in stress-induced emotionality in mice

Neurobiology of Disease

Volumn 46, Issue 2, 2012, Pages 486-496

  Seney, Marianne L ^a   Walsh, Christopher ^a   Stolakis, Ryan ^a   Sibille, Etienne ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Depression; Development; Emotionality; Sex difference; Testosterone; Unpredictable chronic mild stress

Indexed keywords

SEX HORMONE; TESTOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CHRONIC STRESS; CONTROLLED STUDY; EMOTIONAL STRESS; EMOTIONALITY; FEMALE; HORMONAL REGULATION; LOCOMOTION; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE; SEX DIFFERENTIATION;

ANIMALS; ANIMALS, NEWBORN; EMOTIONS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; TESTOSTERONE PROPIONATE;

EID: 84859504791     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.02.014     Document Type: Article

References (61)

1. Angst J., Dobler-Mikola A. Do the diagnostic criteria determine the sex ratio in depression?. J. Affect. Disord. 1984, 7:189-198.
2. Archer J. Rodent sex differences in emotional and related behavior. Behav. Biol. 1975, 14:451-479.
3. Arnold A.P., Chen X. What does the "four core genotypes" mouse model tell us about sex differences in the brain and other tissues?. Front. Neuroendocrinol. 2009, 30:1-9.
4. Arnold A.P., Gorski R.A. Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 1984, 7:413-442.
5. Bodo C., Rissman E.F. The androgen receptor is selectively involved in organization of sexually dimorphic social behaviors in mice. Endocrinology 2008, 149:4142-4150.
6. Breedlove S.M., et al. Masculinization of the female rat spinal cord following a single neonatal injection of testosterone propionate but not estradiol benzoate. Brain Res. 1982, 237:173-181.
7. Caligioni C.S. Assessing reproductive status/stages in mice. Curr. Protoc. Neurosci. 2009, Appendix 4, Appendix 4I.
8. Castro-Costa E., et al. Factors associated with depressive symptoms measured by the 12-item General Health Questionnaire in community-dwelling older adults (The Bambui Health Aging Study). Rev. Bras. Psiquiatr. 2008, 30:104-109.
9. Ciechanowski P.S., et al. Depression and diabetes: impact of depressive symptoms on adherence, function, and costs. Arch. Intern. Med. 2000, 160:3278-3285.
10. Cooke B., et al. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front. Neuroendocrinol. 1998, 19:323-362.
11. Cox K.H., Rissman E.F. Sex differences in juvenile mouse social behavior are influenced by sex chromosomes and social context. Genes Brain Behav. 2011, 10:465-472.
12. De Vries G.J., et al. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 2002, 22:9005-9014.
13. Edgar N.M., et al. Resilient emotionality and molecular compensation in mice lacking the oligodendrocyte-specific gene Cnp1. Transl. Psychiatr. 2011, 1:e42. 10.1038/tp. 2011.40.
14. Frank E., et al. Sex differences in recurrent depression: are there any that are significant?. Am. J. Psychiatry 1988, 145:41-45.
15. Gatewood J.D., et al. Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice. J. Neurosci. 2006, 26:2335-2342.
16. Goel N., Bale T.L. Organizational and activational effects of testosterone on masculinization of female physiological and behavioral stress responses. Endocrinology 2008, 149:6399-6405.
17. Guillamon A., et al. Early effects of gonadal steroids on the neuron number in the medial posterior region and the lateral division of the bed nucleus of the stria terminalis in the rat. Brain Res. Dev. Brain Res. 1988, 44:281-290.
18. Guilloux J.P., et al. Integrated behavioral z-scoring increases the sensitivity and reliability of behavioral phenotyping in mice: relevance to emotionality and sex. J. Neurosci. Methods 2011, 197:21-31.
19. Handa R.J., et al. Differential effects of the perinatal steroid environment on three sexually dimorphic parameters of the rat brain. Biol. Reprod. 1985, 32:855-864.
20. 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.
21. Hisasue S., et al. Control of cell number in the bed nucleus of the stria terminalis of mice: role of testosterone metabolites and estrogen receptor subtypes. J. Sex. Med. 2010, 7:1401-1409.
22. Jacobson C.D., et al. The influence of gonadectomy, androgen exposure, or a gonadal graft in the neonatal rat on the volume of the sexually dimorphic nucleus of the preoptic area. J. Neurosci. 1981, 1:1142-1147.
23. Joeyen-Waldorf J., et al. The roles of sex and serotonin transporter levels in age- and stress-related emotionality in mice. Brain Res. 2009, 1286:84-93.
24. Joffe H., Cohen L.S. Estrogen, serotonin, and mood disturbance: where is the therapeutic bridge?. Biol. Psychiatry 1998, 44:798-811.
25. Kessler R.C., et al. Sex and depression in the National Comorbidity Survey. I: Lifetime prevalence, chronicity and recurrence. J. Affect. Disord. 1993, 29:85-96.
26. Kornstein S.G., et al. Gender differences in chronic major and double depression. J. Affect. Disord. 2000, 60:1-11.
27. Leonardo E.D., Hen R. Anxiety as a developmental disorder. Neuropsychopharmacology 2008, 33:134-140.
28. Lin L.C., et al. A human-mouse conserved sex bias in amygdala gene expression related to circadian clock and energy metabolism. Mol. Brain 2011, 4:18.
29. Lund T.D., et al. Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 2005, 146:797-807.
30. Mann J.J. Neurobiology of suicidal behaviour. Nat. Rev. Neurosci. 2003, 4:819-828.
31. McCarthy M.M., Arnold A.P. Reframing sexual differentiation of the brain. Nat. Neurosci. 2011, 14:677-683.
32. McPhie-Lalmansingh A.A., et al. Sex chromosome complement affects social interactions in mice. Horm. Behav. 2008, 54:565-570.
33. Mong J.A., et al. Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner. J. Neurosci. 1999, 19:1464-1472.
34. Mora S., et al. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996, 21:609-620.
35. Morgan M.A., Pfaff D.W. Effects of estrogen on activity and fear-related behaviors in mice. Horm. Behav. 2001, 40:472-482.
36. Morris J.A., et al. Sexual differentiation of the vertebrate nervous system. Nat. Neurosci. 2004, 7:1034-1039.
37. Moses-Kolko E.L., et al. Transdermal estradiol for postpartum depression: a promising treatment option. Clin. Obstet. Gynecol. 2009, 52:516-529.
38. Murray E.K., et al. Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis. Endocrinology 2009, 150:4241-4247.
39. Murray E.K., et al. Effects of neonatal treatment with valproic acid on vasopressin immunoreactivity and olfactory behaviour in mice. J. Neuroendocrinol. 2011, 23:906-914.
40. Musselman D.L., et al. The relationship of depression to cardiovascular disease: epidemiology, biology, and treatment. Arch. Gen. Psychiatry 1998, 55:580-592.
41. Negri-Cesi P., et al. Sexual differentiation of the brain: role of testosterone and its active metabolites. J. Endocrinol. Invest. 2004, 27:120-127.
42. Nomikos G.G., Spyraki C. Influence of oestrogen on spontaneous and diazepam-induced exploration of rats in an elevated plus maze. Neuropharmacology 1988, 27:691-696.
43. Palanza P. Animal models of anxiety and depression: how are females different?. Neurosci. Biobehav. Rev. 2001, 25:219-233.
44. Perugi G., et al. Gender-mediated clinical features of depressive illness. The importance of temperamental differences. Br. J. Psychiatry 1990, 157:835-841.
45. Phoenix C.H., et al. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959, 65:369-382.
46. Pine D.S., Cohen J.A. Trauma in children and adolescents: risk and treatment of psychiatric sequelae. Biol. Psychiatry 2002, 51:519-531.
47. Pryce C.R., et al. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci. Biobehav. Rev. 2005, 29:649-674.
48. Rubinow D.R., et al. Estrogen-serotonin interactions: implications for affective regulation. Biol. Psychiatry 1998, 44:839-850.
49. Schulz R., et al. Association between depression and mortality in older adults: the Cardiovascular Health Study. Arch. Intern. Med. 2000, 160:1761-1768.
50. Schulz K.M., et al. Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syrian hamster. Horm. Behav. 2004, 45:242-249.
51. Schulz K.M., et al. Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm. Behav. 2009, 55:597-604.
52. Sibille E., et al. Genetic inactivation of the Serotonin(1A) receptor in mice results in downregulation of major GABA(A) receptor alpha subunits, reduction of GABA(A) receptor binding, and benzodiazepine-resistant anxiety. J. Neurosci. 2000, 20:2758-2765.
53. Sibille E., et al. A molecular signature of depression in the amygdala. Am. J. Psychiatry 2009, 166:1011-1024.
54. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 2002, 25:507-536.
55. Simerly R.B., et al. Reversal of the sexually dimorphic distribution of serotonin-immunoreactive fibers in the medial preoptic nucleus by treatment with perinatal androgen. Brain Res. 1985, 340:91-98.
56. Surget A., et al. Corticolimbic transcriptome changes are state-dependent and region-specific in a rodent model of depression and of antidepressant reversal. Neuropsychopharmacology 2009, 34:1363-1380.
57. Viau V., Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991, 129:2503-2511.
58. Voikar V., et al. Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol. Behav. 2001, 72:271-281.
59. Young M.A., et al. Sex differences in the lifetime prevalence of depression: does varying the diagnostic criteria reduce the female/male ratio?. J. Affect. Disord. 1990, 18:187-192.
60. Zuloaga D.G., et al. The organizational role of testicular hormones and the androgen receptor in anxiety-related behaviors and sensorimotor gating in rats. Endocrinology 2011, 152:1572-1581.
61. Zuloaga D.G., et al. Male rats with the testicular feminization mutation of the androgen receptor display elevated anxiety-related behavior and corticosterone response to mild stress. Horm. Behav. 2011, 60:380-388.