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Front Neurosci. 2015 Feb 20;9:37. doi: 10.3389/fnins.2015.00037. eCollection 2015.

Sex hormones affect neurotransmitters and shape the adult female brain during hormonal transition periods.

Frontiers in neuroscience

Claudia Barth, Arno Villringer, Julia Sacher

Affiliations

  1. Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany.
  2. Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany ; Clinic of Cognitive Neurology, University of Leipzig Leipzig, Germany ; Leipzig Research Center for Civilization Diseases, University of Leipzig Leipzig, Germany ; Integrated Research and Treatment Center Adiposity Diseases, University of Leipzig Leipzig, Germany ; Berlin School of Mind and Brain, Mind and Brain Institute Berlin, Germany.
  3. Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany ; Clinic of Cognitive Neurology, University of Leipzig Leipzig, Germany.

PMID: 25750611 PMCID: PMC4335177 DOI: 10.3389/fnins.2015.00037

Abstract

Sex hormones have been implicated in neurite outgrowth, synaptogenesis, dendritic branching, myelination and other important mechanisms of neural plasticity. Here we review the evidence from animal experiments and human studies reporting interactions between sex hormones and the dominant neurotransmitters, such as serotonin, dopamine, GABA and glutamate. We provide an overview of accumulating data during physiological and pathological conditions and discuss currently conceptualized theories on how sex hormones potentially trigger neuroplasticity changes through these four neurochemical systems. Many brain regions have been demonstrated to express high densities for estrogen- and progesterone receptors, such as the amygdala, the hypothalamus, and the hippocampus. As the hippocampus is of particular relevance in the context of mediating structural plasticity in the adult brain, we put particular emphasis on what evidence could be gathered thus far that links differences in behavior, neurochemical patterns and hippocampal structure to a changing hormonal environment. Finally, we discuss how physiologically occurring hormonal transition periods in humans can be used to model how changes in sex hormones influence functional connectivity, neurotransmission and brain structure in vivo.

Keywords: estrogens; hormonal transition periods; neurotransmitters; plasticity; progesterone

References

  1. Brain Res. 2001 Aug 10;910(1-2):55-66 - PubMed
  2. J Psychiatry Neurosci. 2000 May;25(3):262-8 - PubMed
  3. J Neurochem. 1994 May;62(5):1750-6 - PubMed
  4. Cochrane Database Syst Rev. 2013 Feb 28;(2):CD001134 - PubMed
  5. Lancet. 2002 Feb 2;359(9304):378-85 - PubMed
  6. J Neurochem. 1977 Jun;28(6):1221-7 - PubMed
  7. Prog Neurobiol. 1998 Apr;54(5):581-618 - PubMed
  8. Neuropsychopharmacology. 1994 Dec;11(4):245-56 - PubMed
  9. Neurobiol Learn Mem. 2013 Nov;106:221-9 - PubMed
  10. J Neuroendocrinol. 2013 Jun;25(6):560-9 - PubMed
  11. Biol Psychiatry. 2004 Feb 15;55(4):406-12 - PubMed
  12. Maturitas. 2012 Mar;71(3):248-56 - PubMed
  13. J Alzheimers Dis. 2014;42(4):1239-50 - PubMed
  14. Neuropsychopharmacology. 2008 Jan;33(1):73-83 - PubMed
  15. Neuroimage. 2011 Jan 1;54(1):191-202 - PubMed
  16. Glia. 2006 Nov 1;54(6):485-98 - PubMed
  17. Mol Psychiatry. 2013 Apr;18(4):398-9 - PubMed
  18. Annu Rev Neurosci. 2014;37:289-306 - PubMed
  19. EMBO J. 1995 Aug 1;14(15):3741-51 - PubMed
  20. J Neurosci. 2011 Apr 6;31(14):5286-93 - PubMed
  21. Psychoneuroendocrinology. 2006 Sep;31(8):935-47 - PubMed
  22. J Affect Disord. 1993 Oct-Nov;29(2-3):85-96 - PubMed
  23. Neuropsychologia. 2000;38(10):1362-74 - PubMed
  24. Neurobiol Aging. 2003 Sep;24(5):725-32 - PubMed
  25. Cleve Clin J Med. 2004 Feb;71 Suppl 2:S4-10 - PubMed
  26. Arch Gen Psychiatry. 2000 Dec;57(12):1163-4 - PubMed
  27. Int J Fertil Womens Med. 2002 Sep-Oct;47(5):205-10 - PubMed
  28. Endocrine. 2001 Apr;14(3):407-15 - PubMed
  29. Neuropharmacology. 2011 Sep;61(3):348-54 - PubMed
  30. Eur J Pharmacol. 1998 Mar 19;345(2):207-11 - PubMed
  31. Psychol Med. 1998 Jan;28(1):51-61 - PubMed
  32. Brain Res Mol Brain Res. 2005 Apr 27;135(1-2):194-203 - PubMed
  33. Psychoneuroendocrinology. 2011 Sep;36(8):1101-13 - PubMed
  34. Arch Intern Med. 1991 Jan;151(1):97-102 - PubMed
  35. Horm Behav. 2006 Jan;49(1):38-44 - PubMed
  36. Eur Arch Psychiatry Clin Neurosci. 2013 Dec;263(8):685-93 - PubMed
  37. Neuroscience. 2005;134(1):81-95 - PubMed
  38. Brain Res. 2010 Aug 12;1348:55-62 - PubMed
  39. Menopause. 2000 Jul-Aug;7(4):257-65 - PubMed
  40. Steroids. 1999 Jan-Feb;64(1-2):83-91 - PubMed
  41. Front Neuroendocrinol. 2008 Jan;29(1):36-47 - PubMed
  42. Novartis Found Symp. 2000;230:134-45; discussion 145-54 - PubMed
  43. Hippocampus. 2008;18(10):985-8 - PubMed
  44. J Neurosci. 1996 Nov 1;16(21):7021-9 - PubMed
  45. Neuropsychopharmacology. 2012 Jan;37(2):390-401 - PubMed
  46. J Neural Transm Suppl. 1994;44:21-7 - PubMed
  47. Neuroendocrinology. 2005;81(5):294-310 - PubMed
  48. Curr Med Chem. 2014;21(1):113-23 - PubMed
  49. Arch Gen Psychiatry. 2008 Jul;65(7):805-15 - PubMed
  50. Science. 1986 May 23;232(4753):1004-7 - PubMed
  51. Neuroscience. 2011 Sep 15;191:46-54 - PubMed
  52. Annu Rev Pharmacol Toxicol. 2010;50:295-322 - PubMed
  53. J Neurosci. 1982 Feb;2(2):199-205 - PubMed
  54. Horm Behav. 2008 Jan;53(1):61-8 - PubMed
  55. Arch Gen Psychiatry. 2001 Jun;58(6):529-34 - PubMed
  56. Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3870-5 - PubMed
  57. Neuroscience. 2014 Jan 31;258:307-17 - PubMed
  58. Prog Neurobiol. 2001 Jun;64(3):251-67 - PubMed
  59. Nature. 1995 Aug 17;376(6541):572-5 - PubMed
  60. Rev Neurosci. 1994 Jan-Mar;5(1):27-41 - PubMed
  61. Can J Clin Pharmacol. 2009 Winter;16(1):e15-22 - PubMed
  62. Recent Prog Horm Res. 2002;57:357-84 - PubMed
  63. Neuroscience. 2009 Jan 23;158(2):456-64 - PubMed
  64. Neuroscience. 1991;42(2):309-20 - PubMed
  65. Biol Psychiatry. 2012 Apr 1;71(7):633-41 - PubMed
  66. Neuroscience. 2006;138(3):821-9 - PubMed
  67. Nat Neurosci. 2008 Mar;11(3):334-43 - PubMed
  68. J Neurosci. 2009 Oct 14;29(41):12982-93 - PubMed
  69. Neurotoxicology. 2004 Jan;25(1-2):101-15 - PubMed
  70. Hum Brain Mapp. 2014 Sep;35(9):4450-8 - PubMed
  71. J Psychopharmacol. 2013 Dec;27(12):1180-5 - PubMed
  72. J Neurosci. 1996 Nov 1;16(21):6830-8 - PubMed
  73. Arch Gen Psychiatry. 2000 Nov;57(11):1039-45 - PubMed
  74. J Neurosci. 2001 Sep 1;21(17):6532-43 - PubMed
  75. Am J Psychiatry. 2014 Dec 1;171(12):1320-7 - PubMed
  76. N Engl J Med. 1998 Jan 22;338(4):209-16 - PubMed
  77. Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3525-30 - PubMed
  78. Neuropsychopharmacology. 2004 Nov;29(11):2035-45 - PubMed
  79. Arch Gen Psychiatry. 2002 Sep;59(9):851-8 - PubMed
  80. Mol Cell Endocrinol. 2004 Oct 29;226(1-2):33-42 - PubMed
  81. Biol Psychiatry. 2008 Aug 15;64(4):311-9 - PubMed
  82. Hum Reprod. 2002 Jan;17(1):221-7 - PubMed
  83. Am J Obstet Gynecol. 2000 Aug;183(2):414-20 - PubMed
  84. JAMA. 2003 May 28;289(20):2663-72 - PubMed
  85. CNS Spectr. 2008 Aug;13(8):647-62 - PubMed
  86. J Neurobiol. 2005 Jul;64(1):34-46 - PubMed
  87. Proc Natl Acad Sci U S A. 2006 Jul 18;103(29):10923-8 - PubMed
  88. Mol Endocrinol. 2003 May;17(5):831-44 - PubMed
  89. JAMA. 2001 Mar 21;285(11):1489-99 - PubMed
  90. Psychiatry Res. 2013 Dec 30;210(3):1301-3 - PubMed
  91. Arch Gen Psychiatry. 1996 Feb;53(2):175-82 - PubMed
  92. J Natl Cancer Inst. 1999 Jul 7;91(13):1131-7 - PubMed
  93. Cell. 2000 Dec 8;103(6):843-52 - PubMed
  94. J Neurochem. 2007 Dec;103(6):2189-99 - PubMed
  95. Behav Brain Res. 2013 Nov 1;256:520-8 - PubMed
  96. Psychoneuroendocrinology. 2012 Mar;37(3):372-82 - PubMed
  97. Dis Markers. 2011;30(2-3):141-50 - PubMed
  98. JAMA. 2003 May 28;289(20):2651-62 - PubMed
  99. Brain Res. 1987 Jan 6;400(2):353-9 - PubMed
  100. Obstet Gynecol. 2008 May;111(5):1175-82 - PubMed
  101. Trends Pharmacol Sci. 1991 Apr;12(4):141-7 - PubMed
  102. Neurosci Lett. 1990 Oct 16;118(2):169-71 - PubMed
  103. CNS Neurosci Ther. 2010 Jun;16(3):e43-71 - PubMed
  104. Neuroimage. 2006 Aug 1;32(1):457-64 - PubMed
  105. Neuropsychopharmacology. 2014 Apr;39(5):1282-9 - PubMed
  106. J Neurosci. 1990 Apr;10(4):1286-91 - PubMed
  107. J Neurosci. 2008 Dec 10;28(50):13401-10 - PubMed
  108. Arch Gen Psychiatry. 2000 Dec;57(12):1157-62 - PubMed
  109. Exp Clin Psychopharmacol. 2011 Dec;19(6):401-8 - PubMed
  110. Semin Cell Dev Biol. 2000 Feb;11(1):45-52 - PubMed
  111. J Affect Disord. 2003 Mar;74(1):5-13 - PubMed
  112. Curr Top Med Chem. 2002 Aug;2(8):795-816 - PubMed
  113. Arch Gen Psychiatry. 2006 Apr;63(4):375-82 - PubMed
  114. J Biol Chem. 1983 Jan 25;258(2):696-9 - PubMed
  115. Women Birth. 2014 Dec;27(4):e36-42 - PubMed
  116. Brain Res Mol Brain Res. 1997 Apr;45(1):13-23 - PubMed
  117. J Am Acad Child Adolesc Psychiatry. 1994 Jul-Aug;33(6):809-18 - PubMed
  118. Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2231-6 - PubMed
  119. J Steroid Biochem Mol Biol. 2014 Jul;142:90-8 - PubMed
  120. Endocrine. 2008 Jun;33(3):285-93 - PubMed
  121. Cell. 2007 Oct 5;131(1):160-73 - PubMed
  122. J Neural Transm (Vienna). 2014 Aug;121(8):907-24 - PubMed
  123. PLoS One. 2012;7(11):e50167 - PubMed
  124. JAMA Psychiatry. 2013 May;70(5):490-8 - PubMed
  125. Climacteric. 2011 Apr;14(2):244-51 - PubMed
  126. Maturitas. 2010 Dec;67(4):316-20 - PubMed
  127. Br J Pharmacol. 2004 Jan;141(1):92-104 - PubMed
  128. Front Neuroendocrinol. 2006 Dec;27(4):415-35 - PubMed
  129. Int J Obes (Lond). 2008 Jun;32(6):949-58 - PubMed
  130. J Neurosci. 1997 Mar 1;17(5):1848-59 - PubMed
  131. Endocrinology. 2003 May;144(5):2055-67 - PubMed
  132. Eur J Pharmacol. 2001 Apr 27;418(3):157-67 - PubMed
  133. Nature. 1993 Jan 7;361(6407):31-9 - PubMed
  134. Psychoneuroendocrinology. 2014 Jul;45:1-10 - PubMed
  135. Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2237-42 - PubMed
  136. Arch Gen Psychiatry. 2003 Jan;60(1):29-36 - PubMed
  137. Neuroendocrinology. 1993 Jan;57(1):1-6 - PubMed
  138. Neurosci Lett. 1988 Aug 31;91(2):142-7 - PubMed
  139. Neuroreport. 1997 Dec 1;8(17):3817-21 - PubMed
  140. Life Sci. 1983 Apr 25;32(17):2015-21 - PubMed
  141. J Psychiatr Res. 1997 May-Jun;31(3):297-314 - PubMed
  142. Psychopharmacology (Berl). 2011 Feb;213(2-3):265-87 - PubMed
  143. J Neurosci. 2006 Mar 1;26(9):2571-8 - PubMed
  144. Synapse. 2000 Jan;35(1):39-44 - PubMed
  145. Steroids. 2003 Nov;68(10-13):761-70 - PubMed
  146. Ann N Y Acad Sci. 1990;600:427-32; discussion 432-4 - PubMed
  147. JAMA. 2002 Nov 6;288(17):2123-9 - PubMed
  148. Br J Psychiatry. 2003 Oct;183:279-81 - PubMed
  149. Arch Womens Ment Health. 2014 Dec;17(6):569-73 - PubMed
  150. Brain Res Bull. 1987 Jun;18(6):739-47 - PubMed
  151. Front Neuroendocrinol. 2000 Jan;21(1):1-56 - PubMed
  152. Eur Arch Psychiatry Clin Neurosci. 2014 Dec;264(8):729-39 - PubMed
  153. Arch Gen Psychiatry. 2010 May;67(5):468-74 - PubMed
  154. Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):8071-6 - PubMed
  155. Trends Neurosci. 2000 Oct;23(10 Suppl):S34-40 - PubMed
  156. Neurobiol Aging. 2008 Jan;29(1):95-101 - PubMed
  157. Curr Pharm Des. 2006;12(28):3615-30 - PubMed
  158. Menopause. 2006 Jan-Feb;13(1):28-36 - PubMed
  159. Neuropsychopharmacology. 2012 May;37(6):1422-32 - PubMed
  160. Neuroscientist. 2010 Apr;16(2):132-8 - PubMed
  161. Neuroendocrinology. 1984 Aug;39(2):149-55 - PubMed
  162. J Neurophysiol. 1999 Feb;81(2):925-9 - PubMed
  163. J Biol Chem. 1998 Apr 24;273(17):10696-701 - PubMed
  164. J Biol Chem. 1990 Apr 15;265(11):6098-103 - PubMed
  165. Brain Res Mol Brain Res. 1998 Jan;53(1-2):120-9 - PubMed
  166. Biol Psychiatry. 1998 Nov 1;44(9):839-50 - PubMed
  167. Br J Psychiatry. 2000 Dec;177:484-5 - PubMed
  168. Neurology. 2009 Feb 10;72 (6):528-34 - PubMed
  169. Neuron. 2008 Jul 31;59(2):207-13 - PubMed
  170. J Neurophysiol. 2003 Apr;89(4):1929-40 - PubMed
  171. Mol Endocrinol. 2004 Aug;18(8):1859-75 - PubMed
  172. Expert Opin Pharmacother. 2003 Nov;4(11):2065-78 - PubMed
  173. Horm Behav. 2006 Sep;50(3):370-82 - PubMed
  174. Eat Behav. 2006 Aug;7(3):243-51 - PubMed
  175. Arch Gen Psychiatry. 1983 Nov;40(11):1217-23 - PubMed
  176. Gend Med. 2012 Oct;9(5):361-84 - PubMed
  177. Climacteric. 2013 Apr;16(2):214-9 - PubMed
  178. Biol Psychiatry. 2001 May 1;49(9):788-97 - PubMed
  179. Neuropsychopharmacology. 2015 Jan;40(2):429-35 - PubMed
  180. Neuroscience. 2011 Sep 15;191:139-47 - PubMed
  181. JAMA. 2006 Feb 1;295(5):499-507 - PubMed
  182. Brain Res Mol Brain Res. 2001 Jul 13;91(1-2):14-22 - PubMed
  183. Front Neuroendocrinol. 2006 Dec;27(4):404-14 - PubMed
  184. Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12816-21 - PubMed
  185. Neuroscience. 2000;101(3):485-512 - PubMed
  186. Br J Psychiatry. 1994 Apr;164(4):513-6 - PubMed
  187. Biomed Pharmacother. 2009 Mar;63(3):228-35 - PubMed
  188. Front Neuroendocrinol. 2008 May;29(2):238-57 - PubMed
  189. Acta Physiol Scand. 1998 Jan;162(1):77-88 - PubMed
  190. Psychopharmacology (Berl). 2002 Mar;160(3):271-82 - PubMed
  191. Brain Res. 1981 Oct 5;222(1):177-81 - PubMed
  192. J Mol Signal. 2006 Dec 05;1:5 - PubMed
  193. Mol Psychiatry. 2014 May;19(5):588-98 - PubMed
  194. Behav Brain Res. 2001 Jul;122(1):1-9 - PubMed
  195. Neuroimage. 2014 Apr 15;90:24-32 - PubMed
  196. Front Integr Neurosci. 2013 May 23;7:40 - PubMed
  197. Eur Psychiatry. 2002 Jul;17 Suppl 3:294-9 - PubMed
  198. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8836-41 - PubMed
  199. J Neurosci. 1997 Feb 1;17(3):960-74 - PubMed
  200. CNS Drugs. 2003;17(5):325-42 - PubMed
  201. Horm Behav. 2009 May;55(5):646-54 - PubMed
  202. JAMA Psychiatry. 2014 Aug;71(8):873-9 - PubMed
  203. Adv Neurol. 2003;91:107-14 - PubMed
  204. Eur J Pharmacol. 1995 Sep 15;284(1-2):171-6 - PubMed
  205. Can J Exp Psychol. 2008 Dec;62(4):247-60 - PubMed
  206. Soc Personal Psychol Compass. 2012 Jan 1;6(1):1-17 - PubMed
  207. Biol Psychiatry. 2007 Oct 15;62(8):925-33 - PubMed
  208. J Psychiatr Res. 2013 Jun;47(6):816-28 - PubMed
  209. Compr Psychiatry. 2012 Jul;53(5):540-5 - PubMed
  210. Front Synaptic Neurosci. 2010 Jun 10;2:6 - PubMed
  211. Nat Rev Neurosci. 2001 Oct;2(10 ):685-94 - PubMed
  212. Arch Gen Psychiatry. 2006 Nov;63(11):1209-16 - PubMed
  213. Minerva Ginecol. 2013 Dec;65(6):621-30 - PubMed
  214. Science. 1986 Dec 5;234(4781):1261-5 - PubMed
  215. Arch Gen Psychiatry. 2006 Apr;63(4):385-90 - PubMed
  216. Headache. 2006 Sep;46(8):1230-45 - PubMed
  217. J Affect Disord. 2006 Jul;93(1-3):53-60 - PubMed
  218. J Clin Psychiatry. 1998;59 Suppl 15:4-12 - PubMed
  219. Results Probl Cell Differ. 2008;44:87-98 - PubMed
  220. Mol Cell Neurosci. 1993 Feb;4(1):83-92 - PubMed
  221. Brain Res Mol Brain Res. 1998 Aug 31;59(2):205-14 - PubMed
  222. Prog Neurobiol. 2009 Oct;89(2):134-52 - PubMed
  223. Psychoneuroendocrinology. 2013 Dec;38(12):2897-904 - PubMed
  224. Climacteric. 2006 Jun;9(3):181-94 - PubMed
  225. Prog Neurobiol. 2014 Feb;113:88-94 - PubMed
  226. Gynecol Endocrinol. 2007 Mar;23(3):123-30 - PubMed
  227. J Affect Disord. 2014 Jun;161:16-20 - PubMed
  228. Psychopharmacology (Berl). 2006 Jun;186(3):425-33 - PubMed
  229. Steroids. 2000 Oct-Nov;65(10-11):605-12 - PubMed
  230. Mol Psychiatry. 2008 Mar;13(3):325-33 - PubMed
  231. J Neurosci. 1995 Mar;15(3 Pt 1):1835-53 - PubMed
  232. Int J Sports Med. 2001 Oct;22(7):467-81 - PubMed
  233. Neuro Endocrinol Lett. 2006 Oct;27(5):675-8 - PubMed
  234. Front Neurosci. 2013 Sep 19;7:159 - PubMed
  235. Climacteric. 2003 Mar;6(1):2-22 - PubMed
  236. Horm Behav. 2010 Aug;58(3):450-6 - PubMed
  237. J Comp Neurol. 1993 Oct 8;336(2):293-306 - PubMed
  238. Front Neuroendocrinol. 2002 Jan;23(1):41-100 - PubMed
  239. Menopause. 2012 Aug;19(8):894-903 - PubMed
  240. Life Sci. 1993;53(23):1767-77 - PubMed
  241. Neuropsychologia. 2002;40(7):808-16 - PubMed
  242. J Neurosci. 2012 Apr 25;32(17):6000-13 - PubMed
  243. Brain Res. 2006 Dec 18;1126(1):2-26 - PubMed
  244. Eur Radiol. 2013 Jan;23(1):57-64 - PubMed
  245. J Biol Chem. 2002 Aug 9;277(32):28725-32 - PubMed
  246. Biol Psychiatry. 1998 Nov 1;44(9):798-811 - PubMed
  247. J Chem Neuroanat. 2003 Dec;26(4):331-43 - PubMed
  248. Cochrane Database Syst Rev. 2009 Apr 15;(2):CD000402 - PubMed
  249. Annu Rev Sex Res. 2003;14:64-82 - PubMed
  250. Trends Endocrinol Metab. 2010 Sep;21(9):545-52 - PubMed
  251. Psychoneuroendocrinology. 2014 Apr;42:77-88 - PubMed
  252. J Neurosci. 1992 Oct;12(10):3773-80 - PubMed
  253. Prog Neurobiol. 2009 May;88(1):17-31 - PubMed
  254. Curr Med Chem. 2013;20(3):397-404 - PubMed
  255. Front Endocrinol (Lausanne). 2013 Nov 11;4:165 - PubMed
  256. J Neurosci. 1998 Apr 1;18(7):2550-9 - PubMed
  257. Endocrine. 2003 Jun;21(1):67-75 - PubMed
  258. CMAJ. 2000 Jan 25;162(2):225-33 - PubMed
  259. Psychol Med. 2006 Jul;36(7):901-12 - PubMed
  260. J Mol Neurosci. 1993 Winter;4(4):263-75 - PubMed
  261. Menopause. 2014 Feb;21(2):198-206 - PubMed
  262. J Neurochem. 2001 May;77(3):804-11 - PubMed
  263. Proc Soc Exp Biol Med. 1998 Apr;217(4):420-34 - PubMed
  264. Brain Res. 1976 Apr 23;106(2):241-56 - PubMed
  265. J Clin Endocrinol Metab. 1996 Mar;81(3):1076-82 - PubMed
  266. Br J Psychiatry. 1976 Apr;128:379-83 - PubMed
  267. J Clin Diagn Res. 2013 Dec;7(12):2885-8 - PubMed
  268. Horm Behav. 2013 Jul;64(2):203-10 - PubMed
  269. Womens Health (Lond). 2014 Mar;10(2):135-46 - PubMed
  270. Injury. 2012 Jul;43(7):1222-3 - PubMed
  271. Am J Psychiatry. 2012 May;169(5):465-75 - PubMed
  272. Cell Mol Life Sci. 2005 May;62(9):1003-14 - PubMed
  273. Neuron. 1993 Sep;11(3):523-30 - PubMed
  274. Brain Res Bull. 2009 Dec 16;80(6):347-52 - PubMed
  275. Lancet. 2000 Sep 30;356(9236):1131-6 - PubMed
  276. Brain Res Mol Brain Res. 1999 Dec 10;74(1-2):158-66 - PubMed
  277. Exp Neurol. 1997 Oct;147(2):211-20 - PubMed
  278. Endocrine. 1999 Dec;11(3):257-67 - PubMed
  279. Eur Neuropsychopharmacol. 2003 Aug;13(4):228-34 - PubMed
  280. Mol Cell Neurosci. 2012 Mar;49(3):251-62 - PubMed
  281. Psychiatry Res. 2006 Dec 1;148(2-3):185-93 - PubMed
  282. Curr Genomics. 2006;7(8):497-508 - PubMed
  283. Cerebellum. 2012 Jun;11(2):416-7 - PubMed
  284. J Womens Health (Larchmt). 2012 Aug;21(8):830-6 - PubMed
  285. Neuroscience. 2005;135(1):59-72 - PubMed
  286. Behav Brain Res. 2003 Mar 18;140(1-2):1-47 - PubMed
  287. Arch Womens Ment Health. 2004 Oct;7(4):217-21 - PubMed
  288. J Comp Neurol. 2004 Jun 28;474(3):419-26 - PubMed
  289. J Psychiatry Neurosci. 2008 Jul;33(4):331-43 - PubMed
  290. Front Neuroendocrinol. 2008 May;29(2):313-39 - PubMed
  291. Steroids. 2014 Mar;81:74-80 - PubMed
  292. Arch Biochem Biophys. 2011 Apr 1;508(1):1-12 - PubMed
  293. Am J Psychiatry. 2003 Aug;160(8):1522-4 - PubMed
  294. Brain Res. 1990 Jun 11;519(1-2):301-7 - PubMed
  295. Front Pharmacol. 2012 Nov 26;3:195 - PubMed

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