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Reproductive Steroid Regulation of Mood and Behavior

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ABSTRACT

In this article, we examine evidence supporting the role of reproductive steroids in the regulation of mood and behavior in women and the nature of that role. In the first half of the article, we review evidence for the following: (i) the reproductive system is designed to regulate behavior; (ii) from the subcellular to cellular to circuit to behavior, reproductive steroids are powerful neuroregulators; (iii) affective disorders are disorders of behavioral state; and (iv) reproductive steroids affect virtually every system implicated in the pathophysiology of depression. In the second half of the article, we discuss the diagnosis of the three reproductive endocrine‐related mood disorders (premenstrual dysphoric disorder, postpartum depression, and perimenopausal depression) and present evidence supporting the relevance of reproductive steroids to these conditions. Existing evidence suggests that changes in reproductive steroid levels during specific reproductive states (i.e., the premenstrual phase of the menstrual cycle, pregnancy, parturition, and the menopause transition) trigger affective dysregulation in susceptible women, thus suggesting the etiopathogenic relevance of these hormonal changes in reproductive mood disorders. Understanding the source of individual susceptibility is critical to both preventing the onset of illness and developing novel, individualized treatments for reproductive‐related affective dysregulation. © 2016 American Physiological Society. Compr Physiol 6:1135‐1160, 2016e.

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Figure 1. Figure 1. Seventy‐two hours of culture of rat cortical neurons with 100 nm progesterone has opposite effects on neurite length [assessed after staining with microtubule associated protein‐2 (MAP2)] in neurons from male and female animals. The top panel shows cortical neurons stained with MAP2 in male (top) and female (bottom) untreated control rats (left) and those treated with progesterone (right). The bottom panel is a bar graph showing neurite length in male (blue) and female (red) untreated control rats (solid) and those treated with progesterone (striped). Neurite length is greater in female animals compared with males in the absence of progesterone, whereas the opposite is true following exposure to progesterone (L. Zhang et al., unpublished data). ***P < 0.001.
Figure 2. Figure 2. Synthetic pathways for the steroid hormones progesterone, estradiol, and allopregnanolone, reproduced with permission from (328). Note that the same enzymes have multiple actions in the hormone cascade.
Figure 3. Figure 3. The hypothalamic‐pituitary‐gonadal (HPG) axis. The hypothalamus secretes GnRH, which acts on the pituitary gland. In response, the pituitary gland releases the gonadotropins LH and FSH. LH and FSH stimulate the ovaries to produce estrogen and progesterone. Depending on the menstrual cycle phase, estrogen and progesterone provide either positive or negative feedback to the hypothalamus and pituitary.
Figure 4. Figure 4. Recurrence of sadness in women with premenstrual syndrome during estradiol or progesterone add‐back in the context of GnRH agonist‐induced ovarian suppression, reproduced with permission from (275). Ten women with premenstrual syndrome and 15 control women had minimal mood symptoms while receiving leuprolide acetate (a GnRH agonist). In contrast, the women with premenstrual syndrome but not the controls had a significant increase in sadness during the administration of either estradiol or progesterone. Values are the means (±SE) of the seven daily scores on the sadness scale of the Daily Rating Form (83,125) for each of the 8 weeks preceding hormone replacement (leuprolide alone) and during the 4 weeks of estradiol (plus leuprolide) and progesterone (plus leuprolide) replacement. A score of 1 indicates that they symptom was not present, and a score of 6 indicates that it was present in the extreme. P = 0.003 for interaction of treatment condition, diagnostic group, and week.
Figure 5. Figure 5. PET and fMRI activation in a multimodal imaging study of women with PMDD and a comparison group of women, reproduced with permission from (12). Panel A shows the between‐group differences in activation using PET and fMRI. Regions in which patients had greater activation than comparison subjects are shown in pink. Panel B shows the correlations between Global Assessment of Functioning Scale (GAF) scores and activation in patients using PET and fMRI. Regions in which these two measures were negatively correlated (the greater the overactivation, the more severe impairment indicated by GAF scores) are shown in blue.
Figure 6. Figure 6. Mean scores on the Cornell Dysthymia Scale before and after estrogen and progesterone replacement in eight women with a history of postpartum depression and eight healthy comparison women, reproduced with permission from (35). The significant difference between baseline and hormone withdrawal periods in the group with a history of postpartum depression (P < 0.01) is denoted by the symbol (*).
Figure 7. Figure 7. Abnormal maternal behaviors in GABAA receptor δ‐subunit‐deficient mice, reproduced with permission from (181). Panel on right shows that decreased survival of pups born to GABAA receptor δ‐subunit‐deficient (Gabrd+/− and Gabrd−/−) mice is reduced by including a GABAA receptor δ‐subunit‐selective agonist (THIP) in drinking water. Panel on left shows that pups born to Gabrd+/− and Gabrd−/− mice but reared by a surrogate wild‐type mother immediately following birth had an increase in survival compared with wild‐type pups reared by Gabrd+/− and Gabrd−/− surrogate mothers immediately following birth.
Figure 8. Figure 8. The STRAW +10 staging system for reproductive aging in women, reproduced with permission from (130). FMP, final menstrual period.


Figure 1. Seventy‐two hours of culture of rat cortical neurons with 100 nm progesterone has opposite effects on neurite length [assessed after staining with microtubule associated protein‐2 (MAP2)] in neurons from male and female animals. The top panel shows cortical neurons stained with MAP2 in male (top) and female (bottom) untreated control rats (left) and those treated with progesterone (right). The bottom panel is a bar graph showing neurite length in male (blue) and female (red) untreated control rats (solid) and those treated with progesterone (striped). Neurite length is greater in female animals compared with males in the absence of progesterone, whereas the opposite is true following exposure to progesterone (L. Zhang et al., unpublished data). ***P < 0.001.


Figure 2. Synthetic pathways for the steroid hormones progesterone, estradiol, and allopregnanolone, reproduced with permission from (328). Note that the same enzymes have multiple actions in the hormone cascade.


Figure 3. The hypothalamic‐pituitary‐gonadal (HPG) axis. The hypothalamus secretes GnRH, which acts on the pituitary gland. In response, the pituitary gland releases the gonadotropins LH and FSH. LH and FSH stimulate the ovaries to produce estrogen and progesterone. Depending on the menstrual cycle phase, estrogen and progesterone provide either positive or negative feedback to the hypothalamus and pituitary.


Figure 4. Recurrence of sadness in women with premenstrual syndrome during estradiol or progesterone add‐back in the context of GnRH agonist‐induced ovarian suppression, reproduced with permission from (275). Ten women with premenstrual syndrome and 15 control women had minimal mood symptoms while receiving leuprolide acetate (a GnRH agonist). In contrast, the women with premenstrual syndrome but not the controls had a significant increase in sadness during the administration of either estradiol or progesterone. Values are the means (±SE) of the seven daily scores on the sadness scale of the Daily Rating Form (83,125) for each of the 8 weeks preceding hormone replacement (leuprolide alone) and during the 4 weeks of estradiol (plus leuprolide) and progesterone (plus leuprolide) replacement. A score of 1 indicates that they symptom was not present, and a score of 6 indicates that it was present in the extreme. P = 0.003 for interaction of treatment condition, diagnostic group, and week.


Figure 5. PET and fMRI activation in a multimodal imaging study of women with PMDD and a comparison group of women, reproduced with permission from (12). Panel A shows the between‐group differences in activation using PET and fMRI. Regions in which patients had greater activation than comparison subjects are shown in pink. Panel B shows the correlations between Global Assessment of Functioning Scale (GAF) scores and activation in patients using PET and fMRI. Regions in which these two measures were negatively correlated (the greater the overactivation, the more severe impairment indicated by GAF scores) are shown in blue.


Figure 6. Mean scores on the Cornell Dysthymia Scale before and after estrogen and progesterone replacement in eight women with a history of postpartum depression and eight healthy comparison women, reproduced with permission from (35). The significant difference between baseline and hormone withdrawal periods in the group with a history of postpartum depression (P < 0.01) is denoted by the symbol (*).


Figure 7. Abnormal maternal behaviors in GABAA receptor δ‐subunit‐deficient mice, reproduced with permission from (181). Panel on right shows that decreased survival of pups born to GABAA receptor δ‐subunit‐deficient (Gabrd+/− and Gabrd−/−) mice is reduced by including a GABAA receptor δ‐subunit‐selective agonist (THIP) in drinking water. Panel on left shows that pups born to Gabrd+/− and Gabrd−/− mice but reared by a surrogate wild‐type mother immediately following birth had an increase in survival compared with wild‐type pups reared by Gabrd+/− and Gabrd−/− surrogate mothers immediately following birth.


Figure 8. The STRAW +10 staging system for reproductive aging in women, reproduced with permission from (130). FMP, final menstrual period.
References
 1.Abler B, Kumpfmüller D, Grön G, Walter M, Stingl J, Seeringer A. Neural correlates of erotic stimulation under different levels of female sexual hormones. PLoS One 8: e54447, 2013.
 2.Ahokas A, Kaukoranta J, Wahlbeck K, Aito M. Estrogen deficiency in severe postpartum depression: Successful treatment with sublingual physiologic 17beta‐estradiol: A preliminary study. J Clin Psychiatry 62: 332‐336, 2001.
 3.Akwa Y, Purdy RH, Koob GF, Britton KT. The amygdala mediates the anxiolytic‐like effect of the neurosteroid allopregnanolone in rat. Behav Brain Res 106: 119‐125, 1999.
 4.Allen JJB, Urry HL, Hitt SK, Coan JA. The stability of resting frontal electroencephalographic asymmetry in depression. Psychophysiology 41: 269‐280, 2004.
 5.American Psychiatric Association, DSM‐5 Task Force. Diagnostic and Statistical Manual of Mental Disorders: DSM‐5. Arlington, VA: American Psychiatric Association, 2013.
 6.American Psychiatric Association, others. Diagnostic and Statistical Manual of Mental Disorders (5th ed.). Arlington, VA: American Psychiatric Publishing, 2013.
 7.Amin Z, Epperson CN, Constable RT, Canli T. Effects of estrogen variation on neural correlates of emotional response inhibition. NeuroImage 32: 457‐464, 2006.
 8.Andreano JM, Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. NeuroImage 53: 1286‐1293, 2010.
 9.Babayan AH, Kramár EA. Rapid effects of oestrogen on synaptic plasticity: Interactions with actin and its signalling proteins. J Neuroendocrinol 25: 1163‐1172, 2013.
 10.Baehr E, Rosenfeld P, Miller L, Baehr R. Premenstrual dysphoric disorder and changes in frontal alpha asymmetry. Int J Psychophysiol 52: 159‐167, 2004.
 11.Baller EB, Wei S‐M, Kohn PD, Rubinow DR, Alarcón G, Schmidt PJ, Berman KF. Abnormalities of dorsolateral prefrontal function in women with premenstrual dysphoric disorder: A multimodal neuroimaging study. Am J Psychiatry 170: 305‐314, 2013.
 12.Balthazart J, Ball GF. Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29: 241‐249, 2006.
 13.Bannbers E, Gingnell M, Engman J, Morell A, Comasco E, Kask K, Garavan H, Wikström J, Sundström Poromaa I. The effect of premenstrual dysphoric disorder and menstrual cycle phase on brain activity during response inhibition. J Affect Disord 142: 347‐350, 2012.
 14.Barbaccia ML, Roscetti G, Trabucchi M, Purdy RH, Mostallino MC, Concas A, Biggio G. The effects of inhibitors of GABAergic transmission and stress on brain and plasma allopregnanolone concentrations. Br J Pharmacol 120: 1582‐1588, 1997.
 15.Barnes DE, Alexopoulos GS, Lopez OL, Williamson JD, Yaffe K. Depressive symptoms, vascular disease, and mild cognitive impairment: Findings from the cardiovascular health study. Arch Gen Psychiatry 63: 273‐279, 2006.
 16.Bayer J, Bandurski P, Sommer T. Differential modulation of activity related to the anticipation of monetary gains and losses across the menstrual cycle. Eur J Neurosci 38: 3519‐3526, 2013.
 17.Beck AT. Depression: Clinical, Experimental, and Theoretical Aspects. New York: Harper & Row, 1967.
 18.Beck AT. Cognitive Therapy and the Emotional Disorders. New York, NY: Penguin, 1979.
 19.Becker JB. Direct effect of 17β‐estradiol on striatum: Sex differences in dopamine release. Synapse 5: 157‐164, 1990.
 20.Becker JB. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 64: 803‐812, 1999.
 21.Berent‐Spillson A, Persad CC, Love T, Sowers M, Randolph JF, Zubieta J‐K, Smith YR. Hormonal environment affects cognition independent of age during the menopause transition. J Clin Endocrinol Metab 97: E1686‐E1694, 2012.
 22.Berent‐Spillson A, Persad CC, Love T, Tkaczyk A, Wang H, Reame NK, Frey KA, Zubieta JK, Smith YR. Early menopausal hormone use influences brain regions used for visual working memory. Menopause 17: 692‐699, 2010.
 23.Berman KF, Schmidt PJ, Rubinow DR, Danaceau MA, Van Horn JD, Esposito G, Ostrem JL, Weinberger DR. Modulation of cognition‐specific cortical activity by gonadal steroids: A positron‐emission tomography study in women. Proc Natl Acad Sci U S A 94: 8836‐8841, 1997.
 24.Bernstein IH, Rush AJ, Yonkers K, Carmody TJ, Woo A, McConnell K, Trivedi MH. Symptom features of postpartum depression: Are they distinct? Depress Anxiety 25: 20‐26, 2008.
 25.Berridge KC, Valenstein ES. What psychological process mediates feeding evoked by electrical stimulation of the lateral hypothalamus? Behav Neurosci 105: 3‐14, 1991.
 26.Bethea CL, Lu NZ, Gundlah C, Streicher JM. Diverse actions of ovarian steroids in the serotonin neural system. Front Neuroendocrinol 23: 41‐100, 2002.
 27.Bibawi D, Cherry B, Hellige JB. Fluctuations of perceptual asymmetry across time in women and men: Effects related to the menstrual cycle. Neuropsychologia 33: 131‐138, 1995.
 28.Bičíková M, Dibbelt L, Hiill M, Hampl R, Stárka L. Allopregnanolone in women with premenstrual syndrome. Horm Metab Res 30: 227‐229, 2007.
 29.Bitran D, Hilvers RJ, Kellogg CK. Anxiolytic effects of 3α‐hydroxy‐5α[β]‐pregnan‐20‐one: Endogenous metabolites of progesterone that are active at the GABAA receptor. Brain Res 561: 157‐161, 1991.
 30.Bitran D, Purdy RH, Kellog CK. Anxiolytic effect of progesterone is associated with increases in cortical alloprenanolone and GABAA receptor function. Pharmacol Biochem Behav 45: 423‐428, 1993.
 31.Bixo M, Andersson A, Winblad B, Purdy RH, Bäckström T. Progesterone, 5α‐pregnane‐3,20‐dione and 3α‐hydroxy‐5α‐pregnane‐20‐one in specific regions of the human female brain in different endocrine states. Brain Res 764: 173‐178, 1997.
 32.Blanchard JJ, Mueser KT, Bellack AS. Anhedonia, positive and negative affect, and social functioning in schizophrenia. Schizophr Bull 24: 413‐424, 1998.
 33.Blaut A, Paulewicz B, Szastok M, Prochwicz K, Koster E. Are attentional bias and memory bias for negative words causally related? J Behav Ther Exp Psychiatry 44: 293‐299, 2013.
 34.Bloch M, Schmidt PJ, Danaceau M, Murphy J, Nieman L, Rubinow DR. Effects of gonadal steroids in women with a history of postpartum depression. Am J Psychiatry 157: 924‐930, 2000.
 35.Blum M, McEwen BS, Roberts JL. Transcriptional analysis of tyrosine hydroxylase gene expression in the tuberoinfundibular dopaminergic neurons of the rat arcuate nucleus after estrogen treatment. J Biol Chem 262: 817‐821, 1987.
 36.Bortolato M, Devoto P, Roncada P, Frau R, Flore G, Saba P, Pistritto G, Soggiu A, Pisanu S, Zappala A, Ristaldi MS, Tattoli M, Cuomo V, Marrosu F, Barbaccia ML. Isolation rearing‐induced reduction of brain 5α‐reductase expression: Relevance to dopaminergic impairments. Neuropharmacology 60: 1301‐1308, 2011.
 37.Bossé R, Di Paolo T. Dopamine and GABAA receptor imbalance after ovariectomy in rats: Model of menopause. J Psychiatry Neurosci 20: 364‐371, 1995.
 38.Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 108: 16050‐16055, 2011.
 39.Bredemann TM, McMahon LL. 17β Estradiol increases resilience and improves hippocampal synaptic function in helpless ovariectomized rats. Psychoneuroendocrinology 42: 77‐88, 2014.
 40.Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, Finch CE, Morgan TE, Pike CJ, Mack WJ, Stanczyk FZ, Nilsen J. Progesterone receptors: Form and function in brain. Front Neuroendocrinol 29: 313‐339, 2008.
 41.Brötzner CP, Klimesch W, Doppelmayr M, Zauner A, Kerschbaum HH. Resting state alpha frequency is associated with menstrual cycle phase, estradiol and use of oral contraceptives. Brain Res 1577: 36‐44, 2014.
 42.Brown CM, Mulcahey TA, Filipek NC, Wise PM. Production of proinflammatory cytokines and chemokines during neuroinflammation: Novel roles for estrogen receptors α and β. Endocrinology 151: 4916‐4925, 2010.
 43.Bryant DN, Dorsa DM. Roles of estrogen receptors alpha and beta in sexually dimorphic neuroprotection against glutamate toxicity. Neuroscience 170: 1261‐1269, 2010.
 44.Burger H. The menopausal transition—endocrinology. J Sex Med 5: 2266‐2273, 2008.
 45.Byrnes EM, Byrnes JJ, Bridges RS. Increased sensitivity of dopamine systems following reproductive experience in rats. Pharmacol Biochem Behav 68: 481‐489, 2001.
 46.Cardona‐Gomez P, Perez M, Avila J, Garcia‐Segura L, Wandosell F. Estradiol inhibits GSK3 and regulates interaction of estrogen receptors, GSK3, and beta‐catenin in the hippocampus. Mol Cell Neurosci 25: 363‐373, 2004.
 47.Champagne FA, Weaver ICG, Diorio J, Dymov S, Szyf M, Meaney MJ. Maternal care associated with methylation of the estrogen receptor‐α1b promoter and estrogen receptor‐α expression in the medial preoptic area of female offspring. Endocrinology 147: 2909‐2915, 2006.
 48.Champagne F, Diorio J, Sharma S, Meaney MJ. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen‐inducible central oxytocin receptors. Proc Natl Acad Sci U S A 98: 12736‐12741, 2001.
 49.Charkoudian N, Stachenfeld NS. Reproductive hormone influences on thermoregulation in women [Online]. Comprehensive Physiology. John Wiley & Sons, Inc. http://onlinelibrary.wiley.com/doi/10.1002/cphy.c130029/abstract [31 Jul. 2015].
 50.Clarke WP, Maayani S. Estrogen effects on 5‐HT1A receptors in hippocampal membranes from ovariectomized rats: Functional and binding studies. Brain Res 518: 287‐291, 1990.
 51.Clark LA. Temperament as a unifying basis for personality and psychopathology. J Abnorm Psychol 114: 505‐521, 2005.
 52.Clark LA, Watson D. Tripartite model of anxiety and depression: psychometric evidence and taxonomic implications. J Abnorm Psychol 100: 316‐336, 1991.
 53.Cohen LS, Soares CN, Vitonis AF, Otto MW, Harlow BL. Risk for new onset of depression during the menopausal transition: The Harvard Study of Moods and Cycles. Arch Gen Psychiatry 63: 385, 2006.
 54.Coryell W, Akiskal HS, Leon AC, Winokur G, Maser JD, Mueller TI, Keller MB. The time course of nonchronic major depressive disorder: Uniformity across episodes and samples. Arch Gen Psychiatry 51: 405‐410, 1994.
 55.Craig MC, Fletcher PC, Daly EM, Rymer J, Brammer M, Giampietro V, Murphy DGM. Physiological variation in estradiol and brain function: a functional magnetic resonance imaging study of verbal memory across the follicular phase of the menstrual cycle. Horm Behav 53: 503‐508, 2008.
 56.Craig MC, Murphy DG. Estrogen: Effects on normal brain function and neuropsychiatric disorders. Climacteric 10(Suppl 2): 97‐104, 2007.
 57.Cramer OM, Parker CR, Porter JC. Estrogen inhibition of dopamine release into hypophysial portal blood. Endocrinology 104: 419‐422, 1979.
 58.Cunningham M, Gilkeson G. Estrogen receptors in immunity and autoimmunity. Clin Rev Allergy Immunol 40: 66‐73, 2011.
 59.Dalgleish T, Williams JMG, Golden A‐MJ, Perkins N, Barrett LF, Barnard PJ, Yeung CA, Murphy V, Elward R, Tchanturia K, Watkins E. Reduced specificity of autobiographical memory and depression. J Exp Psychol Gen 136: 23‐42, 2007.
 60.Damoiseaux JS, Rombouts SARB, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF. Consistent resting‐state networks across healthy subjects. Proc Natl Acad Sci U S A 103: 13848‐13853, 2006.
 61.Davidson RJ. Anterior electrophysiological asymmetries, emotion, and depression: Conceptual and methodological conundrums. Psychophysiology 35: 607‐614, 1998.
 62.Davidson RJ, Pizzagalli D, Nitschke JB, Putnam K. Depression: Perspectives from affective neuroscience. Annu Rev Psychol 53: 545‐574, 2002.
 63.Debener S, Beauducel A, Nessler D, Brocke B, Heilemann H, Kayser J. Is resting anterior EEG alpha asymmetry a trait marker for depression? Findings for healthy adults and clinically depressed patients. Neuropsychobiology 41: 31‐37, 2000.
 64.Deeks AA, Gibson‐Helm ME, Teede HJ. Anxiety and depression in polycystic ovary syndrome: A comprehensive investigation. Fertil Steril 93: 2421‐2423, 2010.
 65.Deligiannidis KM, Sikoglu EM, Shaffer SA, Frederick B, Svenson AE, Kopoyan A, Kosma CA, Rothschild AJ, Moore CM. GABAergic neuroactive steroids and resting‐state functional connectivity in postpartum depression: A preliminary study. J Psychiatr Res 47: 816‐828, 2013.
 66.Deurveilher S, Rusak B, Semba K. Estradiol and progesterone modulate spontaneous sleep patterns and recovery from sleep deprivation in ovariectomized rats. Sleep 32: 865‐877, 2009.
 67.Dichter GS, Tomarken AJ, Freid CM, Addington S, Shelton RC. Do venlafaxine XR and paroxetine equally influence negative and positive affect? J Affect Disord 85: 333‐339, 2005.
 68.Dinan TG, Barry S, Yatham LN, Mobayed M, O'Hanlon M. The reproducibility of the prolactin response to buspirone: Relationship to the menstrual cycle. Int Clin Psychopharmacol 5: 119‐134, 1990.
 69.Ding EL, Song Y, Malik VS, Liu S. Sex differences of endogenous sex hormones and risk of type 2 diabetes: A systematic review and meta‐analysis. JAMA 295: 1288‐1299, 2006.
 70.Djebaili M, Guo Q, Pettus EH, Hoffman SW, Stein DG. The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats. J Neurotrauma 22: 106‐118, 2005.
 71.Donaldson C, Lam D. Rumination, mood and social problem‐solving in major depression. Psychol Med 34: 1309‐1318, 2004.
 72.Dotson VM, Resnick SM, Zonderman AB. Differential association of concurrent, baseline, and average depressive symptoms with cognitive decline in older adults. Am J Geriatr Psychiatry 16: 318‐330, 2008.
 73.Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, Lanctôt KL. A meta‐analysis of cytokines in major depression. Biol Psychiatry 67: 446‐457, 2010.
 74.Dreher JC, Schmidt PJ, Kohn P, Furman D, Rubinow D, Berman KF. Menstrual cycle phase modulates reward‐related neural function in women. Proc Natl Acad Sci U S A 104: 2465‐2470, 2007.
 75.Drevets WC, Savitz J, Trimble M. The subgenual anterior cingulate cortex in mood disorders. CNS Spectr 13: 663‐681, 2008.
 76.Dubrovsky B. Neurosteroids, neuroactive steroids, and symptoms of affective disorders. Pharmacol Biochem Behav 84: 644‐655, 2006.
 77.Dugard ML, Tremblay‐Leveau H, Mellier D, Caston J. Prenatal exposure to ethinylestradiol elicits behavioral abnormalities in the rat. Dev Brain Res 129: 189‐199, 2001.
 78.Dumas JA, Kutz AM, Naylor MR, Johnson JV, Newhouse PA. Increased memory load‐related frontal activation after estradiol treatment in postmenopausal women. Horm Behav 58: 929‐935, 2010.
 79.Dumas JA, Kutz AM, Naylor MR, Johnson JV, Newhouse PA. Estradiol treatment altered anticholinergic‐related brain activation during working memory in postmenopausal women. NeuroImage 60: 1394‐1403, 2012.
 80.Edler C, Lipson SF, Keel PK. Ovarian hormones and binge eating in bulimia nervosa. Psychol Med 37: 131‐141, 2007.
 81.Elliott R, Dolan RJ, Frith CD. Dissociable functions in the medial and lateral orbitofrontal cortex: Evidence from human neuroimaging studies. Cereb Cortex 10: 308‐317, 2000.
 82.Endicott J, Halbreich U. Retrospective report of premenstrual depressive changes: Factors affecting confirmation by daily ratings. Psychopharmacol Bull 18: 109‐112, 1982.
 83.Engin E, Treit D. The anxiolytic‐like effects of allopregnanolone vary as a function of intracerebral microinfusion site: The amygdala, medial prefrontal cortex, or hippocampus. Behav Pharmacol 18: 461‐470, 2007.
 84.Epperson CN, Haga K, Mason GF, Sellers E, Gueorguieva R, Zhang W, Weiss E, Rothman DL, Krystal JH. Cortical gamma‐aminobutyric acid levels across the menstrual cycle in healthy women and those with premenstrual dysphoric disorder: A proton magnetic resonance spectroscopy study. Arch Gen Psychiatry 59: 851‐858, 2002.
 85.Epperson CN, Gueorguieva R, Czarkowski KA, Stiklus S, Sellers E, Krystal JH, Rothman DL, Mason GF. Preliminary evidence of reduced occipital GABA concentrations in puerperal women: A 1H‐MRS study. Psychopharmacology (Berl) 186: 425‐433, 2006.
 86.Epperson CN, Steiner M, Hartlage SA, Eriksson E, Schmidt PJ, Jones I, Yonkers KA. Premenstrual dysphoric disorder: Evidence for a new category for DSM‐5. Am J Psychiatry 169: 465‐475, 2012.
 87.Eser D, Schüle C, Baghai TC, Romeo E, Rupprecht R. Neuroactive steroids in depression and anxiety disorders: Clinical studies. Neuroendocrinology 84: 244‐254, 2006.
 88.Eshel N, Roiser JP. Reward and punishment processing in depression. Biol Psychiatry 68: 118‐124, 2010.
 89.Etgen AM, Ansonoff MA, Quesada A. Mechanisms of ovarian steroid regulation of norepinephrine receptor‐mediated signal transduction in the hypothalamus: Implications for female reproductive physiology. Horm Behav 40: 169‐177, 2001.
 90.Fassnacht M, Schlenz N, Schneider SB, Wudy SA, Allolio B, Arlt W. Beyond adrenal and ovarian androgen generation: Increased peripheral 5α‐reductase activity in women with polycystic ovary syndrome. J Clin Endocrinol Metab 88: 2760‐2766, 2003.
 91.Fink G, Sumner BEH. Oestrogen and mental state. Nature 383: 306‐306, 1996.
 92.Fitzgerald PB, Oxley TJ, Laird AR, Kulkarni J, Egan GF, Daskalakis ZJ. An analysis of functional neuroimaging studies of dorsolateral prefrontal cortical activity in depression. Psychiatry Res 148: 33‐45, 2006.
 93.Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8: 700‐711, 2007.
 94.Franz WB. Basic review: Endocrinology of the normal menstrual cycle. Prim Care 15: 607‐616, 1988.
 95.Freeman E, Rickels K, Sondheimer S, Polansky M. Ineffectiveness of progesterone suppository treatment for premenstrual syndrome. JAMA 264: 349‐353, 1990.
 96.Freeman E, Rickels K, Sondheimer S, Polansky M. A double‐blind trial of oral progesterone, alprazolam, and placebo in treatment of severe premenstrual syndrome. JAMA 274: 51‐57, 1995.
 97.Freeman EW, Frye CA, Rickels K, Martin PAG, Smith SS. Allopregnanolone levels and symptom improvement in severe premenstrual syndrome. J Clin Psychopharmacol 22: 516‐520, 2002.
 98.Freeman EW, Sammel MD, Lin H, Nelson DB. Associations of hormones and menopausal status with depressed mood in women with no history of depression. Arch Gen Psychiatry 63: 375‐382, 2006.
 99.Fröhlich F. Endogenous and exogenous electric fields as modifiers of brain activity: Rational design of noninvasive brain stimulation with transcranial alternating current stimulation. Dialogues Clin Neurosci 16: 93‐102, 2014.
 100.Frye CA, Walf AA, Rhodes ME, Harney JP. Progesterone enhances motor, anxiolytic, analgesic, and antidepressive behavior of wild‐type mice, but not those deficient in type 1 5 alpha‐reductase. Brain Res 1004: 116‐124, 2004.
 101.Furuta M, Numakawa T, Chiba S, Ninomiya M, Kajiyama Y, Adachi N, Akema T, Kunugi H. Estrogen, predominantly via estrogen receptor α, attenuates postpartum‐induced anxiety‐ and depression‐like behaviors in female rats. Endocrinology 154: 3807‐3816, 2013.
 102.Gardner A, Boles RG. Beyond the serotonin hypothesis: Mitochondria, inflammation and neurodegeneration in major depression and affective spectrum disorders. Prog Neuropsychopharmacol Biol Psychiatry 35: 730‐743, 2011.
 103.Gardner A, Johansson A, Wibom R, Nennesmo I, von Döbeln U, Hagenfeldt L, Hällström T. Alterations of mitochondrial function and correlations with personality traits in selected major depressive disorder patients. J Affect Disord 76: 55‐68, 2003.
 104.Gavin KM, Gibbons E, Stavros A, Nakamura T, Villalon KL, Kohrt WM. Ovarian hormone suppression with estradiol add‐back therapy in premenopausal women reduces dynamic HPA axis activity. Endocrine Reviews 34S: SUN‐55, 2013.
 105.Gavin NI, Gaynes BN, Lohr KN, Meltzer‐Brody S, Gartlehner G, Swinson T. Perinatal depression: A systematic review of prevalence and incidence. Obstet Gynecol 106: 1071‐1083, 2005.
 106.Geary N, Trace D, McEwen B, Smith GP. Cyclic estradiol replacement increases the satiety effect of CCK‐8 in ovariectomized rats. Physiol Behav 56: 281‐289, 1994.
 107.Genazzani AR, Petraglia F, Bernardi F, Casarosa E, Salvestroni C, Tonetti A, Nappi RE, Luisi S, Palumbo M, Purdy RH, Luisi M. Circulating levels of allopregnanolone in humans: Gender, age, and endocrine influences. J Clin Endocrinol Metab 83: 2099‐2103, 1998.
 108.Gillies GE, McArthur S. Estrogen actions in the brain and the basis for differential action in men and women: A case for sex‐specific medicines. Pharmacol Rev 62: 155‐198, 2010.
 109.Gingnell M, Morell A, Bannbers E, Wikström J, Sundström Poromaa I. Menstrual cycle effects on amygdala reactivity to emotional stimulation in premenstrual dysphoric disorder. Horm Behav 62: 400‐406, 2012.
 110.Girdler SS, Straneva PA, Light KC, Pedersen CA, Morrow AL. Allopregnanolone levels and reactivity to mental stress in premenstrual dysphoric disorder. Biol Psychiatry 49: 788‐797, 2001.
 111.Goldstein JM, Jerram M, Poldrack R, Ahern T, Kennedy DN, Seidman LJ, Makris N. Hormonal cycle modulates arousal circuitry in women using functional magnetic resonance imaging. J Neurosci Off J Soc Neurosci 25: 9309‐9316, 2005.
 112.Goodyer IM, Herbert J, Altham PM, Pearson J, Secher SM, Shiers HM. Adrenal secretion during major depression in 8‐ to 16‐year‐olds, I. Altered diurnal rhythms in salivary cortisol and dehydroepiandrosterone (DHEA) at presentation. Psychol Med 26: 245‐256, 1996.
 113.Gotlib IH. EEG alpha asymmetry, depression, and cognitive functioning. Cogn Emot 12: 449‐478, 1998.
 114.Gotlib IH, Krasnoperova E, Yue DN, Joormann J. Attentional biases for negative interpersonal stimuli in clinical depression. J Abnorm Psychol 113: 127‐135, 2004.
 115.Gotlib IH, Whiffen VE, Mount JH, Milne K, Cordy NI. Prevalence rates and demographic characteristics associated with depression in pregnancy and the postpartum. J Consult Clin Psychol 57: 269‐274, 1989.
 116.Greendale GA, Huang M‐H, Wight RG, Seeman T, Luetters C, Avis NE, Johnston J, Karlamangla AS. Effects of the menopause transition and hormone use on cognitive performance in midlife women. Neurology 72: 1850‐1857, 2009.
 117.Green PS, Gridley KE, Simpkins JW. Nuclear estrogen receptor‐independent neuroprotection by estratrienes: A novel interaction with glutathione. Neuroscience 84: 7‐10, 1998.
 118.Gregoire AJ, Kumar R, Everitt B, Henderson AF, Studd JW. Transdermal oestrogen for treatment of severe postnatal depression. Lancet 347: 930‐933, 1996.
 119.Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, Kenna H, Reiss AL, Schatzberg AF. Resting‐state functional connectivity in major depression: Abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62: 429‐437, 2007.
 120.Grieve SM, Korgaonkar MS, Koslow SH, Gordon E, Williams LM. Widespread reductions in gray matter volume in depression. NeuroImage Clin 3: 332‐339, 2013.
 121.Grimm S, Beck J, Schuepbach D, Hell D, Boesiger P, Bermpohl F, Niehaus L, Boeker H, Northoff G. Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: An fMRI study in severe major depressive disorder. Biol Psychiatry 63: 369‐376, 2008.
 122.Grimm S, Boesiger P, Beck J, Schuepbach D, Bermpohl F, Walter M, Ernst J, Hell D, Boeker H, Northoff G. Altered negative BOLD responses in the default‐mode network during emotion processing in depressed subjects. Neuropsychopharmacology 34: 932‐943, 2009.
 123.Grodstein F, Lifford K, Resnick NM, Curhan GC. Postmenopausal hormone therapy and risk of developing urinary incontinence. Obstet Gynecol 103: 254‐260, 2004.
 124.Grodstein F, Manson JE, Stampfer MJ. Hormone therapy and coronary heart disease: The role of time since menopause and age at hormone initiation. J Womens Health 15: 35‐44, 2006.
 125.Halbreich U, Endicott J, Lesser J. The clinical diagnosis and classification of premenstrual changes. Can J Psychiatry Rev Can Psychiatr 30: 489‐497, 1985.
 126.Hamilton JP, Etkin A, Furman DJ, Lemus MG, Johnson RF, Gotlib IH. Functional neuroimaging of major depressive disorder: A meta‐analysis and new integration of base line activation and neural response data. Am J Psychiatry 169: 693‐703, 2012.
 127.Hampson E. Variations in sex‐related cognitive abilities across the menstrual cycle. Brain Cogn 14: 26‐43, 1990.
 128.Hampson E, Kimura D. Reciprocal effects of hormonal fluctuations on human motor and perceptual‐spatial skills. Behav Neurosci 102: 456‐459, 1988.
 129.Han SJ, DeMayo FJ, Xu J, Tsai SY, Tsai M‐J, O'Malley BW. Steroid receptor coactivator (SRC)‐1 and SRC‐3 differentially modulate tissue‐specific activation functions of the progesterone receptor. Mol Endocrinol 20: 45‐55, 2006.
 130.Harlow SD, Gass M, Hall JE, Lobo R, Maki P, Rebar RW, Sherman S, Sluss PM, de Villiers TJ. Executive summary of the Stages of Reproductive Aging Workshop + 10: addressing the unfinished agenda of staging reproductive aging. Fertil Steril 97: 843‐851, 2012.
 131.Hausmann M, Hamm JP, Waldie KE, Kirk IJ. Sex hormonal modulation of interhemispheric transfer time. Neuropsychologia 51: 1734‐1741, 2013.
 132.He J, Evans C‐O, Hoffman SW, Oyesiku NM, Stein DG. Progesterone and allopregnanolone reduce inflammatory cytokines after traumatic brain injury. Exp Neurol 189: 404‐412, 2004.
 133.Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Ström A, Treuter E, Warner M, Gustafsson J‐Å. Estrogen receptors: How do they signal and what are their targets. Physiol Rev 87: 905‐931, 2007.
 134.Henriques JB, Davidson RJ. Regional brain electrical asymmetries discriminate between previously depressed and healthy control subjects. J Abnorm Psychol 99: 22‐31, 1990.
 135.Henriques JB, Davidson RJ. Left frontal hypoactivation in depression. J Abnorm Psychol 100: 535‐545, 1991.
 136.Herman JP, Cullinan WE. Neurocircuitry of stress: Central control of the hypothalamo–pituitary–adrenocortical axis. Trends Neurosci 20: 78‐84, 1997.
 137.Heuser I, Deuschle M, Luppa P, Schweiger U, Standhardt H, Weber B. Increased diurnal plasma concentrations of dehydroepiandrosterone in depressed patients. J Clin Endocrinol Metab 83: 3130‐3133, 1998.
 138.Holländer A, Hausmann M, Hamm JP, Corballis MC. Sex hormonal modulation of hemispheric asymmetries in the attentional blink. J Int Neuropsychol Soc 11: 263‐272, 2005.
 139.Howe ML, Malone C. Mood‐congruent true and false memory: Effects of depression. Memory 19: 192‐201, 2011.
 140.Jennings JH, Sparta DR, Stamatakis AM, Ung RL, Pleil KE, Kash TL, Stuber GD. Distinct extended amygdala circuits for divergent motivational states. Nature 496: 224‐228, 2013.
 141.Jollant F, Bellivier F, Leboyer M, Astruc B, Torres S, Verdier R, Castelnau D, Malafosse A, Courtet P. Impaired decision making in suicide attempters. Am J Psychiatry 162: 304‐310, 2005.
 142.Joormann J, Gotlib IH. Selective attention to emotional faces following recovery from depression. J Abnorm Psychol 116: 80‐85, 2007.
 143.Joormann J, Gotlib IH. Updating the contents of working memory in depression: Interference from irrelevant negative material. J Abnorm Psychol 117: 182‐192, 2008.
 144.Kaiser S, Roth A, Rentrop M, Friederich H‐C, Bender S, Weisbrod M. Intra‐individual reaction time variability in schizophrenia, depression and borderline personality disorder. Brain Cogn 66: 73‐82, 2008.
 145.Karkanias GB, Etgen AM. Estradiol attenuates α2‐adrenoceptor‐mediated inhibition of hypothalamic norepinephrine release. J Neurosci 13: 3448‐3455, 1993.
 146.Karkanias GB, Li C‐S, Etgen AM. Estradiol reduction of α2‐adrenoceptor binding in female rat cortex is correlated with decreases in α2A/D‐adrenoceptor messenger RNA. Neuroscience 81: 593‐597, 1997.
 147.Kehoe P, Mallinson K, McCormick CM, Frye CA. Central allopregnanolone is increased in rat pups in response to repeated, short episodes of neonatal isolation. Dev Brain Res 124: 133‐136, 2000.
 148.Kendall D, Stancel G, Enna S. Imipramine: Effect of ovarian steroids on modifications in serotonin receptor binding. Science 211: 1183‐1185, 1981.
 149.Kenna HA, Rasgon NL, Geist C, Small G, Silverman D. Thalamo‐basal ganglia connectivity in postmenopausal women receiving estrogen therapy. Neurochem Res 34: 234‐237, 2009.
 150.Kiss Á, Delattre AM, Pereira SIR, Carolino RG, Szawka RE, Anselmo‐Franci JA, Zanata SM, Ferraz AC. 17β‐Estradiol replacement in young, adult and middle‐aged female ovariectomized rats promotes improvement of spatial reference memory and an antidepressant effect and alters monoamines and BDNF levels in memory‐ and depression‐related brain areas. Behav Brain Res 227: 100‐108, 2012.
 151.Klasen M, Kreifelts B, Chen Y‐H, Seubert J, Mathiak K. Neural processing of emotion in multimodal settings. Front Hum Neurosci 8: 822, 2014.
 152.Klatzkin RR, Leslie Morrow A, Light KC, Pedersen CA, Girdler SS. Associations of histories of depression and PMDD diagnosis with allopregnanolone concentrations following the oral administration of micronized progesterone. Psychoneuroendocrinology 31: 1208‐1219, 2006.
 153.Klimesch W. α‐band oscillations, attention, and controlled access to stored information. Trends Cogn Sci 16: 606‐617, 2012.
 154.Klump KL, Keel PK, Culbert KM, Edler C. Ovarian hormones and binge eating: Exploring associations in community samples. Psychol Med 38: 1749‐1757, 2008.
 155.Koenigs M, Grafman J. The functional neuroanatomy of depression: Distinct roles for ventromedial and dorsolateral prefrontal cortex. Behav Brain Res 201: 239‐243, 2009.
 156.Korgaonkar MS, Fornito A, Williams LM, Grieve SM. Abnormal structural networks characterize major depressive disorder: A connectome analysis. Biol Psychiatry 76: 567‐574, 2014.
 157.Korol DL. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol Learn Mem 82: 309‐323, 2004.
 158.Koster EHW, De Lissnyder E, Derakshan N, De Raedt R. Understanding depressive rumination from a cognitive science perspective: The impaired disengagement hypothesis. Clin Psychol Rev 31: 138‐145, 2011.
 159.Koster EHW, De Raedt R, Goeleven E, Franck E, Crombez G. Mood‐congruent attentional bias in dysphoria: Maintained attention to and impaired disengagement from negative information. Emot Wash DC 5: 446‐455, 2005.
 160.Kow L‐M, Pfaff DW. Mapping of neural and signal transduction pathways for lordosis in the search for estrogen actions on the central nervous system. Behav Brain Res 92: 169‐180, 1998.
 161.Kravitz HM, Zhao X, Bromberger JT, Gold EB, Hall MH, Matthews KA, Sowers MFR. Sleep disturbance during the menopausal transition in a multi‐ethnic community sample of women. Sleep 31: 979‐990, 2008.
 162.Krystal JH, Sanacora G, Blumberg H, Anand A, Charney DS, Marek G, Epperson CN, Goddard A, Mason GF. Glutamate and GABA systems as targets for novel antidepressant and mood‐stabilizing treatments. Mol Psychiatry 7: S71‐S80, 2002.
 163.Kulkarni J, de Castella A, Fitzgerald PB, Gurvich CT, Bailey M, Bartholomeusz C, Burger H. Estrogen in severe mental illness: A potential new treatment approach. Arch Gen Psychiatry 65: 955‐960, 2008.
 164.Kulkarni J, Gurvich C, Lee SJ, Gilbert H, Gavrilidis E, de Castella A, Berk M, Dodd S, Fitzgerald PB, Davis SR. Piloting the effective therapeutic dose of adjunctive selective estrogen receptor modulator treatment in postmenopausal women with schizophrenia. Psychoneuroendocrinology 35: 1142‐1147, 2010.
 165.De Kwaasteniet B, Ruhe E, Caan M, Rive M, Olabarriaga S, Groefsema M, Heesink L, van Wingen G, Denys D. Relation between structural and functional connectivity in major depressive disorder. Biol Psychiatry 74: 40‐47, 2013.
 166.Larson EB, Roth ME, Anker JJ, Carroll ME. Effect of short‐ vs. long‐term estrogen on reinstatement of cocaine‐seeking behavior in female rats. Pharmacol Biochem Behav 82: 98‐108, 2005.
 167.Law Smith MJ, Deady DK, Moore FR, Jones BC, Cornwell RE, Stirrat M, Lawson JF, Feinberg DR, Perrett DI. Maternal tendencies in women are associated with estrogen levels and facial femininity. Horm Behav 61: 12‐16, 2012.
 168.Lawrie TA, Hofmeyr GJ, De Jager M, Berk M, Paiker J, Viljoen E. A double‐blind randomised placebo controlled trial of postnatal norethisterone enanthate: The effect on postnatal depression and serum hormones. Br J Obstet Gynaecol 105: 1082‐1090, 1998.
 169.Lemogne C, le Bastard G, Mayberg H, Volle E, Bergouignan L, Lehéricy S, Allilaire J‐F, Fossati P. In search of the depressive self: Extended medial prefrontal network during self‐referential processing in major depression. Soc Cogn Affect Neurosci 4: 305‐312, 2009.
 170.Leonard BE. The immune system, depression and the action of antidepressants. Prog Neuropsychopharmacol Biol Psychiatry 25: 767‐780, 2001.
 171.Leuchter AF, Cook IA, Jin Y, Phillips B. The relationship between brain oscillatory activity and therapeutic effectiveness of transcranial magnetic stimulation in the treatment of major depressive disorder. Front Hum Neurosci 7: 37, 2013.
 172.Lin I‐M, Tsai Y‐C, Peper E, Yen C‐F. Depressive mood and frontal alpha asymmetry during the luteal phase in premenstrual dysphoric disorder. J Obstet Gynaecol Res 39: 998‐1006, 2013.
 173.Lipovka Y, Konhilas JP. Estradiol activates AMPK through interaction with extrogen receptor beta (15.4). FASEB J 28: 15.4, 2014.
 174.Liston C, Chen AC, Zebley BD, Drysdale AT, Gordon R, Leuchter B, Voss HU, Casey BJ, Etkin A, Dubin MJ. Default mode network mechanisms of transcranial magnetic stimulation in depression. Biol Psychiatry 76: 517‐526, 2014.
 175.Liu S, Zhang N, Guo Y, Zhao R, Shi T, Feng S, Wang S, Yang Q, Li X, Wu Y, Ma L, Hou Y, Xiong L, Zhang W, Zhao M. G‐protein‐coupled receptor 30 mediates rapid neuroprotective effects of Estrogen via depression of NR2B‐containing NMDA receptors. J Neurosci 32: 4887‐4900, 2012.
 176.Lonard DM, O'Malley BW. Nuclear receptor coregulators: Judges, juries, and executioners of cellular regulation. Mol Cell 27: 691‐700, 2007.
 177.Lonard DM, O'Malley BW. Nuclear receptor coregulators: Modulators of pathology and therapeutic targets. Nat Rev Endocrinol 8: 598‐604, 2012.
 178.Lu J, Xu Y, Sheng H, Tang Z, Ni X. 17β‐Estradiol replacement to ovariectomized rats ameliorates depression‐like behavior (876.2). FASEB J 28: 876.2, 2014.
 179.Maguire J, Ferando I, Simonsen C, Mody I. Excitability changes related to GABAA receptor plasticity during pregnancy. J Neurosci 29: 9592‐9601, 2009.
 180.Maguire JL, Stell BM, Rafizadeh M, Mody I. Ovarian cycle‐linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8: 797‐804, 2005.
 181.Maguire J, Mody I. GABAAR plasticity during pregnancy: Relevance to postpartum depression. Neuron 59: 207‐213, 2008.
 182.Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM. Steroid hormone metabolites are barbiturate‐like modulators of the GABA receptor. Science 232: 1004‐1007, 1986.
 183.Manji HK, Quiroz JA, Sporn J, Payne JL, Denicoff K, A Gray N, Zarate CA, Jr., Charney DS. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult‐to‐treat depression. Biol Psychiatry 53: 707‐742, 2003.
 184.Marcondes FK, Miguel KJ, Melo LL, Spadari‐Bratfisch RC. Estrous cycle influences the response of female rats in the elevated plus‐maze test. Physiol Behav 74: 435‐440, 2001.
 185.Mars RB, Neubert F‐X, Noonan MP, Sallet J, Toni I, Rushworth MFS. On the relationship between the “default mode network” and the “social brain.” Front Hum Neurosci 6: 189, 2012.
 186.Mayberg HS, Brannan SK, Tekell JL, Silva JA, Mahurin RK, McGinnis S, Jerabek PA. Regional metabolic effects of fluoxetine in major depression: Serial changes and relationship to clinical response. Biol Psychiatry 48: 830‐843, 2000.
 187.Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, Schwalb JM, Kennedy SH. Deep brain stimulation for treatment‐resistant depression. Neuron 45: 651‐660, 2005.
 188.McCARTHY MM. Estradiol and the developing brain. Physiol Rev 88: 91‐134, 2008.
 189.McCarthy MM, Arnold AP. Reframing sexual differentiation of the brain. Nat Neurosci 14: 677‐683, 2011.
 190.McClure RES, Barha CK, Galea LAM. 17β‐Estradiol, but not estrone, increases the survival and activation of new neurons in the hippocampus in response to spatial memory in adult female rats. Horm Behav 63: 144‐157, 2013.
 191.McDermott LM, Ebmeier KP. A meta‐analysis of depression severity and cognitive function. J Affect Disord 119: 1‐8, 2009.
 192.McEwen BS. Invited Review: Estrogens effects on the brain: Multiple sites and molecular mechanisms. J Appl Physiol 91: 2785‐2801, 2001.
 193.McEwen BS, Akama KT, Spencer‐Segal JL, Milner TA, Waters EM. Estrogen effects on the brain: Actions beyond the hypothalamus via novel mechanisms. Behav Neurosci 126: 4‐16, 2012.
 194.McQueen JK, Wilson H, Dow RC. Oestradiol‐17β increases serotonin transporter (SERT) binding sites and SERT mRNA expression in discrete regions of female rat brain. J Physiol 495: 114, 1996.
 195.Mead LA, Hampson E. A sex difference in turning bias in humans. Behav Brain Res 78: 73‐79, 1996.
 196.Micevych P, Dominguez R. Membrane estradiol signaling in the brain. Front Neuroendocrinol 30: 315‐327, 2009.
 197.Michael A, Jenaway A, Paykel ES, Herbert J. Altered salivary dehydroepiandrosterone levels in major depression in adults. Biol Psychiatry 48: 989‐995, 2000.
 198.Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24: 167‐202, 2001.
 199.Moffitt TE, Harrington H, Caspi A, Kim‐Cohen J, Goldberg D, Gregory AM, Poulton R. Depression and generalized anxiety disorder: Cumulative and sequential comorbidity in a birth cohort followed prospectively to age 32 years. Arch Gen Psychiatry 64: 651‐660, 2007.
 200.Mogenson GJ, Stevenson JAF. Drinking induced by electrical stimulation of the lateral hypothalamus. Exp Neurol 17: 119‐127, 1967.
 201.Monteleone P, Luisi S, Tonetti A, Bernardi F, Genazzani AD, Luisi M, Petraglia F, Genazzani AR. Allopregnanolone concentrations and premenstrual syndrome. Eur J Endocrinol Eur Fed Endocr Soc 142: 269‐273, 2000.
 202.Mook DG, Kenney NJ, Roberts S, Nussbaum AI, Rodier WII. Ovarian‐adrenal interactions in regulation of body weight by female rats. J Comp Physiol Psychol 81: 198‐211, 1972.
 203.Mooradian AD. Antioxidant properties of steroids. J Steroid Biochem Mol Biol 45: 509‐511, 1993.
 204.Moreau JL, Bourson A, Jenck F, Martin JR, Mortas P. Curative effects of the atypical antidepressant mianserin in the chronic mild stress‐induced anhedonia model of depression. J Psychiatry Neurosci 19: 51‐56, 1994.
 205.Moreau JL, Jenck F, Martin JR, Mortas P, Haefely WE. Antidepressant treatment prevents chronic unpredictable mild stress‐induced anhedonia as assessed by ventral tegmentum self‐stimulation behavior in rats. Eur Neuropsychopharmacol 2: 43‐49, 1992.
 206.Morissette M, Di Paolo T. Sex and estrous cycle variations of rat striatal dopamine uptake sites. Neuroendocrinology 58: 16‐22, 1993.
 207.Moritz S, Gläscher J, Brassen S. Investigation of mood‐congruent false and true memory recognition in depression. Depress Anxiety 21: 9‐17, 2005.
 208.Moscovitch DA, Santesso DL, Miskovic V, McCabe RE, Antony MM, Schmidt LA. Frontal EEG asymmetry and symptom response to cognitive behavioral therapy in patients with social anxiety disorder. Biol Psychol 87: 379‐385, 2011.
 209.Moses EL, Drevets WC, Smith G, Mathis CA, Kalro BN, Butters MA, Leondires MP, Greer PJ, Lopresti B, Loucks TL, Berga SL. Effects of estradiol and progesterone administration on human serotonin 2A receptor binding: A PET study. Biol Psychiatry 48: 854‐860, 2000.
 210.Moses‐Kolko EL, Fraser D, Wisner KL, James JA, Saul AT, Fiez JA, Phillips ML. Rapid habituation of ventral striatal response to reward receipt in postpartum depression. Biol Psychiatry 70: 395‐399, 2011.
 211.Moses‐Kolko EL, Perlman SB, Wisner KL, James J, Saul AT, Phillips ML. Abnormally reduced dorsomedial prefrontal cortical activity and effective connectivity with amygdala in response to negative emotional faces in postpartum depression. Am J Psychiatry 167: 1373‐1380, 2010.
 212.Napoli A, Powers JB, Valenstein ES. Hormonal induction of behavioral estrus modified by electrical stimulation of hypothalamus. Physiol Behav 9: 115‐117, 1972.
 213.Nelson BD, McGowan SK, Sarapas C, Robison‐Andrew EJ, Altman SE, Campbell ML, Gorka SM, Katz AC, Shankman SA. Biomarkers of threat and reward sensitivity demonstrate unique associations with risk for psychopathology. J Abnorm Psychol 122: 662‐671, 2013.
 214.Nelson BP, Henriet RP, Holt AW, Bopp KC, Houser AP, Allgood OE, Turner JE. The role of estrogen in the developmental appearance of sensory‐motor behaviors in the zebrafish (Danio rerio): The characterization of the “listless” model. Brain Res 1222: 118‐128, 2008.
 215.Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM. Neurobiology of depression. Neuron 34: 13‐25, 2002.
 216.Nolen‐Hoeksema S. The role of rumination in depressive disorders and mixed anxiety/depressive symptoms. J Abnorm Psychol 109: 504‐511, 2000.
 217.Notelovitz M, Lenihan Jr JP, McDermott M, Kerber IJ, Nanavati N, Arce J‐C. Initial 17β‐estradiol dose for treating vasomotor symptoms1. Obstet Gynecol 95: 726‐731, 2000.
 218.Ogawa S, Chan J, Gustafsson J‐Å, Korach KS, Pfaff DW. Estrogen increases locomotor activity in mice through estrogen receptor α: Specificity for the type of activity. Endocrinology 144: 230‐239, 2003.
 219.Ogawa S, Lee TM, Kay AR, Tank DW. Brain Magnetic Resonance Imaging with Contrast Dependent on Blood Oxygenation. Proceedings of the National Academy of Sciences 87(24): 9868‐9872, 1990.
 220.O'Hara MW. Postpartum Depression: Causes and Consequences. New York: Springer‐Verlag, 1995.
 221.O'Hara MW, Schlechte JA, Lewis DA, Varner MW. Controlled prospective study of postpartum mood disorders: Psychological, environmental, and hormonal variables. J Abnorm Psychol 100: 63‐73, 1991.
 222.O'Hara MW, Swain AM. Rates and risk of postpartum depression—A meta‐analysis. Int Rev Psychiatry 8: 37‐54, 1996.
 223.O'Malley BW. The “fourth dimension” of gene transcription. Mol Endocrinol 23: 587‐589, 2009.
 224.Ottowitz WE, Derro D, Dougherty DD, Lindquist MA, Fischman AJ, Hall JE. FDG‐PET analysis of amygdalar‐cortical network covariance during pre‐ versus post‐menopausal estrogen levels: Potential relevance to resting state networks, mood, and cognition. Neuro Endocrinol Lett 29: 467‐474, 2008.
 225.Ottowitz WE, Siedlecki KL, Lindquist MA, Dougherty DD, Fischman AJ, Hall JE. Evaluation of prefrontal‐hippocampal effective connectivity following 24 hours of estrogen infusion: an FDG‐PET study. Psychoneuroendocrinology 33: 1419‐1425, 2008.
 226.Paelecke‐Habermann Y, Pohl J, Leplow B. Attention and executive functions in remitted major depression patients. J Affect Disord 89: 125‐135, 2005.
 227.Di Paolo T, Poyet P, Labrie F. Prolactin and estradiol increase striatal dopamine receptor density in intact, castrated and hypophysectomized rats. Prog Neuropsychopharmacol Biol Psychiatry 6: 377‐382, 1982.
 228.Papousek I, Weiss EM, Schulter G, Fink A, Reiser EM, Lackner HK. Prefrontal EEG alpha asymmetry changes while observing disaster happening to other people: Cardiac correlates and prediction of emotional impact. Biol Psychol 103: 189‐194, 2014.
 229.Park H‐J, Friston K. Structural and functional brain networks: From connections to cognition. Science 342: 1238411, 2013.
 230.Pasqualini C, Leviel V, Guibert B, Faucon‐Biguet N, Kerdelhué B. Inhibitory actions of acute estradiol treatment on the activity and quantity of tyrosine hydroxylase in the median eminence of ovariectomized rats. J Neuroendocrinol 3: 575‐580, 1991.
 231.Patchev VK, Hassan AHS, Holsboer F, Almeida OFX. The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid‐like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15: 533‐540, 1996.
 232.Patchev VK, Shoaib M, Holsboer F, Almeida OFX. The neurosteroid tetrahydroprogesterone counteracts corticotropin‐releasing hormone‐induced anxiety and alters the release and gene expression of corticotropin‐releasing hormone in the rat hypothalamus. Neuroscience 62: 265‐271, 1994.
 233.Pearlstein T, Yonkers KA, Fayyad R, Gillespie JA. Pretreatment pattern of symptom expression in premenstrual dysphoric disorder. J Affect Disord 85: 275‐282, 2005.
 234.Pecins‐Thompson M, Brown NA, Bethea CL. Regulation of serotonin re‐uptake transporter mRNA expression by ovarian steroids in rhesus macaques. Mol Brain Res 53: 120‐129, 1998.
 235.Petitti N, Etgen AM. Alpha 1‐adrenoceptor augmentation of beta‐stimulated cAMP formation is enhanced by estrogen and reduced by progesterone in rat hypothalamic slices. J Neurosci 10: 2842‐2849, 1990.
 236.Pfaff DW. Luteinizing hormone‐releasing factor potentiates lordosis behavior in hypophysectomized ovariectomized female rats. Science 182: 1148‐1149, 1973.
 237.Pfaff DW, Sakuma Y. Facilitation of the lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus. J Physiol 288: 189‐202, 1979.
 238.Piferrer F, Baker IJ, Donaldson EM. Effects of natural, synthetic, aromatizable, and nonaromatizable androgens in inducing male sex differentiation in genotypic female Chinook Salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol 91: 59‐65, 1993.
 239.Pletzer BA, Kerschbaum HH. 50 years of hormonal contraception—time to find out, what it does to our brain. Front Neurosci 8: 256, 2014.
 240.Polo‐Kantola P, Erkkola R, Helenius H, Irjala K, Polo O. When does estrogen replacement therapy improve sleep quality? Am J Obstet Gynecol 178: 1002‐1009, 1998.
 241.Power RF, Mani SK, Codina J, Conneely OM, O'Malley BW. Dopaminergic and ligand‐independent activation of steroid hormone receptors. Science 254: 1636‐1639, 1991.
 242.Protopopescu X, Pan H, Altemus M, Tuescher O, Polanecsky M, McEwen B, Silbersweig D, Stern E. Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. Proc Natl Acad Sci U S A 102: 16060‐16065, 2005.
 243.Protopopescu X, Tuescher O, Pan H, Epstein J, Root J, Chang L, Altemus M, Polanecsky M, McEwen B, Stern E, Silbersweig D. Toward a functional neuroanatomy of premenstrual dysphoric disorder. J Affect Disord 108: 87‐94, 2008.
 244.Pyter LM, Kelly SD, Harrell CS, Neigh GN. Sex differences in the effects of adolescent stress on adult brain inflammatory markers in rats. Brain Behav Immun 30: 88‐94, 2013.
 245.Raison CL, Capuron L, Miller AH. Cytokines sing the blues: Inflammation and the pathogenesis of depression. Trends Immunol 27: 24‐31, 2006.
 246.Van Randenborgh A, de Jong‐Meyer R, Hüffmeier J. Decision making in depression: Differences in decisional conflict between healthy and depressed individuals. Clin Psychol Psychother 17: 285‐298, 2010.
 247.Rapkin AJ, Berman SM, Mandelkern MA, Silverman DHS, Morgan M, London ED. Neuroimaging evidence of cerebellar involvement in premenstrual dysphoric disorder. Biol Psychiatry 69: 374‐380, 2011.
 248.Rapkin AJ, Morgan M, Goldman L, Brann DW, Simone D, Mahesh VB. Progesterone metabolite allopregnanolone in women with premenstrual syndrome. Obstet Gynecol 90: 709‐714, 1997.
 249.Rapp PR, Morrison JH, Roberts JA. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 23: 5708‐5714, 2003.
 250.Raymond V, Beaulieu M, Labrie F, Boissier J. Potent antidopaminergic activity of estradiol at the pituitary level on prolactin release. Science 200: 1173‐1175, 1978.
 251.Roca CA, Schmidt PJ, Altemus M, Deuster P, Danaceau MA, Putnam K, Rubinow DR. Differential menstrual cycle regulation of hypothalamic‐pituitary‐adrenal axis in women with premenstrual syndrome and controls. J Clin Endocrinol Metab 88: 3057‐3063, 2003.
 252.Roca CA, Schmidt PJ, Deuster PA, Danaceau MA, Altemus M, Putnam K, Chrousos GP, Nieman LK, Rubinow DR. Sex‐related differences in stimulated hypothalamic‐pituitary‐adrenal axis during induced gonadal suppression. J Clin Endocrinol Metab 90: 4224‐4231, 2005.
 253.Rode C, Wagner M, Güntürkün O. Menstrual cycle affects functional cerebral asymmetries. Neuropsychologia 33: 855‐865, 1995.
 254.Romeo E, Ströhle A, Spalletta G, di Michele F, Hermann B, Holsboer F, Pasini A, Rupprecht R. Effects of antidepressant treatment on neuroactive steroids in major depression. Am J Psychiatry 155: 910‐913, 1998.
 255.Rossmanith WG, Ruebberdt W. What causes hot flushes? The neuroendocrine origin of vasomotor symptoms in the menopause. Gynecol Endocrinol 25: 303‐314, 2009.
 256.Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SAA, Howard BV, Johnson KC, Kotchen JM, Ockene J, Writing Group for the Women's Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: Principal results From the Women's Health Initiative randomized controlled trial. JAMA 288: 321‐333, 2002.
 257.Rossouw JE, Prentice RL, Manson JE, Wu L, Barad D, Barnabei VM, Ko M, LaCroix AZ, Margolis KL, Stefanick ML. Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. JAMA 297: 1465‐1477, 2007.
 258.Roy M‐A, Neale MC, Pedersen NL, Mathé AA, Kendler KS. A twin study of generalized anxiety disorder and major depression. Psychol Med 25: 1037‐1049, 1995.
 259.Rubinow DR. Reproductive steroids in context. Arch Women's Ment Health 8: 1‐5, 2005.
 260.Rubinow DR, Girdler SS. Hormones, heart disease, and health: Individualized medicine versus throwing the baby out with the bathwater. Depress Anxiety 28: 282‐296, 2011.
 261.Rubinow DR, Schmidt PJ. Gonadal steroids, brain, and behavior: Role of context. Dialogues Clin Neurosci 4: 123‐137, 2002.
 262.Rubinow DR, Schmidt PJ, Roca CA. Estrogen–serotonin interactions: Implications for affective regulation. Biol Psychiatry 44: 839‐850, 1998.
 263.Rumberg B, Baars A, Fiebach J, Ladd ME, Forsting M, Senf W, Gizewski ER. Cycle and gender‐specific cerebral activation during a verb generation task using fMRI: Comparison of women in different cycle phases, under oral contraception, and men. Neurosci Res 66: 366‐371, 2010.
 264.Sadaghiani S, Scheeringa R, Lehongre K, Morillon B, Giraud A‐L, Kleinschmidt A. Intrinsic connectivity networks, alpha oscillations, and tonic alertness: A simultaneous electroencephalography/functional magnetic resonance imaging study. J Neurosci 30: 10243‐10250, 2010.
 265.Sampson GA. Premenstrual syndrome: A double‐blind controlled trial of progesterone and placebo. Br J Psychiatry 135: 209‐215, 1979.
 266.Sato K, Akaishi T, Matsuki N, Ohno Y, Nakazawa K. beta‐Estradiol induces synaptogenesis in the hippocampus by enhancing brain‐derived neurotrophic factor release from dentate gyrus granule cells. Brain Res 1150: 108‐120, 2007.
 267.Sayeed I, Parvez S, Wali B, Siemen D, Stein DG. Direct inhibition of the mitochondrial permeability transition pore: A possible mechanism for better neuroprotective effects of allopregnanolone over progesterone. Brain Res 1263: 165‐173, 2009.
 268.Schiller C. The hormone withdrawal hypothesis of postpartum depression: A translational approach [Online]. Theses Diss. http://ir.uiowa.edu/etd/1261.
 269.Schiller CE, Schmidt PJ, Rubinow DR. Allopregnanolone as a mediator of affective switching in reproductive mood disorders. Psychopharmacology (Berl) 231: 3557‐3567, 2014.
 270.Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, Axmacher N, Joe AY, Kreft M, Lenartz D, Sturm V. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33: 368‐377, 2008.
 271.Schmidt P, Daly RC, Bloch M, Smith MJ, Danaceau MA, St Clair LS, Murphy JH, Haq N, Rubinow DR. Dehydroepiandrosterone monotherapy in midlife‐onset major and minor depression. Arch Gen Psychiatry 62: 154‐162, 2005.
 272.Schmidt PJ, Ben Dor R, Martinez PE, Guerrieri, GM, Harsh VL, Thompson K, Koziol DE, Nieman LK, Rubinow DR. Effects of estradiol withdrawal on mood in women with past perimenopausal depression: A randomized clinical trial. JAMA Psychiatry 72: 714‐726, 2015.
 273.Schmidt PJ, Haq N, Rubinow DR. A longitudinal rvaluation of the relationship between reproductive status and mood in perimenopausal women. Am J Psychiatry 161: 2238‐2244, 2004.
 274.Schmidt PJ, Murphy JH, Haq N, Danaceau MA, St Clair L. Basal plasma hormone levels in depressed perimenopausal women. Psychoneuroendocrinology 27: 907‐920, 2002.
 275.Schmidt PJ, Nieman L, Danaceau MA, Tobin MB, Roca CA, Murphy JH, Rubinow DR. Estrogen replacement in perimenopause‐related depression: A preliminary report. Am J Obstet Gynecol 183: 414‐420, 2000.
 276.Schmidt PJ, Nieman LK, Danaceau MA, Adams LF, Rubinow DR. Differential behavioral effects of gonadal steroids in women with and in those without premenstrual syndrome. N Engl J Med 338: 209‐216, 1998.
 277.Schmidt PJ, Purdy RH, Moore PH, Paul SM, Rubinow DR. Circulating levels of anxiolytic steroids in the luteal phase in women with premenstrual syndrome and in control subjects. J Clin Endocrinol Metab 79: 1256‐1260, 1994.
 278.Schöning S, Engelien A, Kugel H, Schäfer S, Schiffbauer H, Zwitserlood P, Pletziger E, Beizai P, Kersting A, Ohrmann P, Greb RR, Lehmann W, Heindel W, Arolt V, Konrad C. Functional anatomy of visuo‐spatial working memory during mental rotation is influenced by sex, menstrual cycle, and sex steroid hormones. Neuropsychologia 45: 3203‐3214, 2007.
 279.Schoning S, Zwitserlood P, Engelien A, Behnken A, Kugel H, Schiffbauer H, Lipina K, Pachur C, Kersting A, Dannlowski U, Baune BT, Zwanzger P, Reker T, Heindel W, Arolt V, Konrad C. Working‐memory fMRI reveals cingulate hyperactivation in euthymic major depression. Hum Brain Mapp 30: 2746‐2756, 2009.
 280.Schüle C, Baghai TC, di Michele F, Eser D, Pasini A, Schwarz M, Rupprecht R, Romeo E. Effects of combination treatment with mood stabilizers and mirtazapine on plasma concentrations of neuroactive steroids in depressed patients. Psychoneuroendocrinology 32: 669‐680, 2007.
 281.Schüle C, Eser D, Baghai TC, Nothdurfter C, Kessler JS, Rupprecht R. Neuroactive steroids in affective disorders: Target for novel antidepressant or anxiolytic drugs? Neuroscience 191: 55‐77, 2011.
 282.Schüle C, Romeo E, Uzunov DP, Eser D, di Michele F, Baghai TC, Pasini A, Schwarz M, Kempter H, Rupprecht R. Influence of mirtazapine on plasma concentrations of neuroactive steroids in major depression and on 3α‐hydroxysteroid dehydrogenase activity. Mol Psychiatry 11: 261‐272, 2005.
 283.Shansky RM, Bender G, Arnsten AFT. Estrogen prevents norepinephrine alpha‐2a receptor reversal of stress‐induced working memory impairment. Stress 12: 457‐463, 2009.
 284.Sheline YI, Barch DM, Price JL, Rundle MM, Vaishnavi SN, Snyder AZ, Mintun MA, Wang S, Coalson RS, Raichle ME. The default mode network and self‐referential processes in depression. Proc Natl Acad Sci U S A 106: 1942‐1947, 2009.
 285.Sheline YI, Price JL, Yan Z, Mintun MA. Resting‐state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proc Natl Acad Sci U S A 107: 11020‐11025, 2010.
 286.Shen H, Gong QH, Aoki C, Yuan M, Ruderman Y, Dattilo M, Williams K, Smith SS. Reversal of neurosteroid effects at α4β2δ GABAA receptors triggers anxiety at puberty. Nat Neurosci 10: 469‐477, 2007.
 287.Shimizu E, Hashimoto K, Okamura N, Koike K, Komatsu N, Kumakiri C, Nakazato M, Watanabe H, Shinoda N, Okada S, Iyo M. Alterations of serum levels of brain‐derived neurotrophic factor (BDNF) in depressed patients with or without antidepressants. Biol Psychiatry 54: 70‐75, 2003.
 288.Shirayama Y, Muneoka K, Fukumoto M, Tadokoro S, Fukami G, Hashimoto K, Iyo M. Infusions of allopregnanolone into the hippocampus and amygdala, but not into the nucleus accumbens and medial prefrontal cortex, produce antidepressant effects on the learned helplessness rats. Hippocampus 21: 1105‐1113, 2011.
 289.Shulman LM. Is there a connection between estrogen and Parkinson's disease? Parkinsonism Relat Disord 8: 289‐295, 2002.
 290.Sichel DA, Cohen LS, Robertson LM, Ruttenberg A, Rosenbaum JF. Prophylactic estrogen in recurrent postpartum affective disorder. Biol Psychiatry 38: 814‐818, 1995.
 291.Silverman ME, Loudon H, Safier M, Protopopescu X, Leiter G, Liu X, Goldstein M. Neural dysfunction in postpartum depression: An fMRI pilot study. CNS Spectr 12: 853‐862, 2007.
 292.Singer CA, Rogers KL, Strickland TM, Dorsa DM. Estrogen protects primary cortical neurons from glutamate toxicity. Neurosci Lett 212: 13‐16, 1996.
 293.Sisk CL, Zehr JL. Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 26: 163‐174, 2005.
 294.Smith CT, Sierra Y, Oppler SH, Boettiger CA. Ovarian cycle effects on immediate reward selection bias in humans: A role for estradiol. J Neurosci 34: 5468‐5476, 2014.
 295.Smith MJ, Adams LF, Schmidt PJ, Rubinow DR, Wassermann EM. Effects of ovarian hormones on human cortical excitability. Ann Neurol 51: 599‐603, 2002.
 296.Smith MJ, Adams LF, Schmidt PJ, Rubinow DR, Wassermann EM. Abnormal luteal phase excitability of the motor cortex in women with premenstrual syndrome. Biol Psychiatry 54: 757‐762, 2003.
 297.Smith SS. Female sex steroid hormones: From receptors to networks to performance—Actions on the sensorimotor system. Prog Neurobiol 44: 55‐86, 1994.
 298.Smith SS, Gong QH, Hsu FC, Markowitz RS, French‐Mullen JM, Li X. GABA(A) receptor alpha4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature 392: 926‐930, 1998.
 299.Smith SS, Gong QH, Li X, Moran MH, Bitran D, Frye CA, Hsu F‐C. Withdrawal from 3α‐OH‐5α‐Pregnan‐20‐One using a pseudopregnancy model alters the kinetics of hippocampal GABAA‐gated current and increases the GABAAreceptor α4 subunit in association with increased anxiety. J Neurosci 18: 5275‐5284, 1998.
 300.Smith SS, Ruderman Y, Frye C, Homanics G, Yuan M. Steroid withdrawal in the mouse results in anxiogenic effects of 3alpha,5beta‐THP: A possible model of premenstrual dysphoric disorder. Psychopharmacology (Berl) 186: 323‐333, 2006.
 301.Sohrabji F, Greene LA, Miranda RC, Toran‐Allerand CD. Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. J Neurobiol 25: 974‐988, 1994.
 302.Sohrabji F, Miranda RC, Toran‐Allerand CD. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 14: 459‐471, 1994.
 303.Sporns O. Structure and function of complex brain networks. Dialogues Clin Neurosci 15: 247‐262, 2013.
 304.Sripada RK, Marx CE, King AP, Rampton JC, Ho SS, Liberzon I. Allopregnanolone elevations following pregnenolone administration are associated with enhanced activation of emotion regulation neurocircuits. Biol Psychiatry 73: 1045‐1053, 2013.
 305.Stachenfeld NS, Silva C, Keefe DL. Estrogen modifies the temperature effects of progesterone. J Appl Physiol 88: 1643‐1649, 2000.
 306.Steinberg EM, Rubinow DR, Bartko JJ, Fortinsky PM, Haq N, Thompson K, Schmidt PJ. A cross‐sectional evaluation of perimenopausal depression. J Clin Psychiatry 69: 973‐980, 2008.
 307.Stewart JL, Bismark AW, Towers DN, Coan JA, Allen JJB. Resting frontal EEG asymmetry as an endophenotype for depression risk: Sex‐specific patterns of frontal brain asymmetry. J Abnorm Psychol 119: 502‐512, 2010.
 308.Stirone C, Duckles SP, Krause DN, Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 68: 959‐965, 2005.
 309.Stowe ZN, Hostetter AL, Newport DJ. The onset of postpartum depression: Implications for clinical screening in obstetrical and primary care. Am J Obstet Gynecol 192: 522‐526, 2005.
 310.Strekalova T, Gorenkova N, Schunk E, Dolgov O, Bartsch D. Selective effects of citalopram in a mouse model of stress‐induced anhedonia with a control for chronic stress. Behav Pharmacol 17: 271‐287, 2006.
 311.Ströhle A, Romeo E, Hermann B, Pasini A, Spalletta G, di Michele F, Holsboer F, Rupprecht R. Concentrations of 3α‐reduced neuroactive steroids and their precursors in plasma of patients with major depression and after clinical recovery. Biol Psychiatry 45: 274‐277, 1999.
 312.Sumner BE, Grant KE, Rosie R, Hegele‐Hartung C, Fritzemeier K‐H, Fink G. Effects of tamoxifen on serotonin transporter and 5‐hydroxytryptamine2A receptor binding sites and mRNA levels in the brain of ovariectomized rats with or without acute estradiol replacement. Mol Brain Res 73: 119‐128, 1999.
 313.Sumner BEH, Fink G. Estrogen increases the density of 5‐Hydroxytryptamine2A receptors in cerebral cortex and nucleus accumbens in the female rat. J Steroid Biochem Mol Biol 54: 15‐20, 1995.
 314.Sunday L, Tran MM, Krause DN, Duckles SP. Estrogen and progestagens differentially modulate vascular proinflammatory factors. Am J Physiol Endocrinol Metab 291: E261‐E267, 2006.
 315.Sundström I, Bäckström T. Citalopram increases pregnanolone sensitivity in patients with premenstrual syndrome: An open trial. Psychoneuroendocrinology 23: 73‐88, 1998.
 316.Sundström I, Nyberg S, Bäckström T. Patients with premenstrual syndrome have reduced sensitivity to midazolam compared to control subjects. Neuropsychopharmacology 17: 370‐381, 1997.
 317.Sundström Poromaa I, Smith S, Gulinello M. GABA receptors, progesterone and premenstrual dysphoric disorder. Arch Womens Ment Health 6: 23‐41, 2003.
 318.Su TP, Schmidt PJ, Danaceau M, Murphy DL, Rubinow DR. Effect of menstrual cycle phase on neuroendocrine and behavioral responses to the serotonin agonist m‐chlorophenylpiperazine in women with premenstrual syndrome and controls. J Clin Endocrinol Metab 82: 1220‐1228, 1997.
 319.Tang Y, Janssen WGM, Hao J, Roberts JA, McKay H, Lasley B, Allen PB, Greengard P, Rapp PR, Kordower JH, Hof PR, Morrison JH. Estrogen replacement increases spinophilin‐immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cereb Cortex 14: 215‐223, 2004.
 320.Terauchi M, Obayashi S, Akiyoshi M, Kato K, Matsushima E, Kubota T. Effects of oral estrogen and hypnotics on Japanese peri‐ and postmenopausal women with sleep disturbance. J Obstet Gynaecol Res 37: 741‐749, 2011.
 321.Thibodeau R, Jorgensen RS, Kim S. Depression, anxiety, and resting frontal EEG asymmetry: A meta‐analytic review. J Abnorm Psychol 115: 715‐729, 2006.
 322.Thimm M, Weis S, Hausmann M, Sturm W. Menstrual cycle effects on selective attention and its underlying cortical networks. Neuroscience 258: 307‐317, 2014.
 323.Thomas M, Bland DA, Clarke CH, Cunningham KA. Estrogen regulation of serotonin (5‐HT) transporter and 5‐HT1A receptor mRNA in female rat brain. Abstr Soc Neurosci 23: 1501, 1997.
 324.Tiemstra JD, Patel K. Hormonal therapy in the management of premenstrual syndrome. J Am Board Fam Pract 11: 378‐381, 1998.
 325.Tomarken AJ, Dichter GS, Garber J, Simien C. Resting frontal brain activity: Linkages to maternal depression and socio‐economic status among adolescents. Biol Psychol 67: 77‐102, 2004.
 326.Tom SE, Anderson ML, Landis CA, Aiello Bowles EJ, Woods NF, Reed SD, Newton KM, Buist DSM. Sleep problems after short‐term hormone therapy suspension: Secondary analysis of a randomized trial. Menopause N Y N 18: 1184‐1190, 2011.
 327.Tsang K‐L, Ho S‐L, Lo S‐K. Estrogen improves motor disability in parkinsonian postmenopausal women with motor fluctuations. Neurology 54: 2292‐2298, 2000.
 328.Tsutsui K, Ukena K, Sakamoto H, Okuyama S‐I, Haraguchi S. Biosynthesis, mode of action, and functional significance of neurosteroids in the Purkinje cell. Front Endocrinol 2: 61, 2011.
 329.Tuohy A, McVey C. Subscales measuring symptoms of non‐specific depression, anhedonia, and anxiety in the Edinburgh Postnatal Depression Scale. Br J Clin Psychol 47: 153‐169, 2008.
 330.Ungar S, Makman MH, Morris SA, Etgen AM. Estrogen uncouples beta‐adrenergic receptor from the stimulatory guanine nucleotide‐binding protein in female rat hypothalamus. Endocrinology 133: 2818‐2826, 1993.
 331.Uzunova V, Sheline Y, Davis JM, Rasmusson A, Uzunov DP, Costa E, Guidotti A. Increase in the cerebrospinal fluid content of neurosteroids in patients with unipolar major depression who are receiving fluoxetine or fluvoxamine. Proc Natl Acad Sci U S A 95: 3239‐3244, 1998.
 332.Vasudevan N, Kow L‐M, Pfaff DW. Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line. Proc Natl Acad Sci U S A 98: 12267‐12271, 2001.
 333.Vasudevan N, Pfaff DW. Non‐genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol 29: 238‐257, 2008.
 334.Vesga‐Lopez O, Blanco C, Keyes K, Olfson M, Grant BF, Hasin DS. Psychiatric disorders in pregnant and postpartum women in the United States. Arch Gen Psychiatry 65: 805‐815, 2008.
 335.Wainwright NWJ, Surtees PG. Childhood adversity, gender and depression over the life‐course. J Affect Disord 72: 33‐44, 2002.
 336.Walf AA, Frye CA. ERβ‐selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 30: 1598‐1609, 2005.
 337.Wang M, Seippel L, Purdy RH, Bãckström T. Relationship between symptom severity and steroid variation in women with premenstrual syndrome: study on serum pregnenolone, pregnenolone sulfate, 5 alpha‐pregnane‐3,20‐dione and 3 alpha‐hydroxy‐5 alpha‐pregnan‐20‐one. J Clin Endocrinol Metab 81: 1076‐1082, 1996.
 338.Wang X‐J. Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90: 1195‐1268, 2010.
 339.Waters EM, Simerly RB. Estrogen induces caspase‐dependent cell death during hypothalamic development. J Neurosci 29: 9714‐9718, 2009.
 340.Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: The PANAS scales. J Pers Soc Psychol 54: 1063‐1070, 1988.
 341.Watson D, O'Hara MW, Simms LJ, Kotov R, Chmielewski M, McDade‐Montez EA, Gamez W, Stuart S. Development and validation of the Inventory of Depression and Anxiety Symptoms (IDAS). Psychol Assess 19: 253‐268, 2007.
 342.Watson D, Weber K, Assenheimer JS, Clark LA, Strauss ME, McCormick RA. Testing a tripartite model: I. Evaluating the convergent and discriminant validity of anxiety and depression symptom scales. J Abnorm Psychol 104: 3‐14, 1995.
 343.Weiser MJ, Foradori CD, Handa RJ. Estrogen receptor beta in the brain: From form to function. Brain Res Rev 57: 309‐320, 2008.
 344.Weis S, Hausmann M, Stoffers B, Sturm W. Dynamic changes in functional cerebral connectivity of spatial cognition during the menstrual cycle. Hum Brain Mapp 32: 1544‐1556, 2011.
 345.Weis S, Hausmann M, Stoffers B, Vohn R, Kellermann T, Sturm W. Estradiol modulates functional brain organization during the menstrual cycle: An analysis of interhemispheric inhibition. J Neurosci 28: 13401‐13410, 2008.
 346.Wesström J, Nilsson S, Sundström‐Poromaa I, Ulfberg J. Restless legs syndrome among women: Prevalence, co‐morbidity and possible relationship to menopause. Climacteric 11: 422‐428, 2008.
 347.Whitfield‐Gabrieli S, Ford JM. Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol 8: 49‐76, 2012.
 348.Wieland S, Lan NC, Mirasedeghi S, Gee KW. Anxiolytic activity of the progesterone metabolite 5α‐pregnan‐3α‐ol‐20‐one. Brain Res 565: 263‐268, 1991.
 349.Williams JMG, Barnhofer T, Crane C, Beck AT. Problem solving deteriorates following mood challenge in formerly depressed patients with a history of suicidal ideation. J Abnorm Psychol 114: 421‐431, 2005.
 350.Van Wingen GA, van Broekhoven F, Verkes RJ, Petersson KM, Backstrom T, Buitelaar JK, Fernandez G. Progesterone selectively increases amygdala reactivity in women. Mol Psychiatry 13: 325‐333, 2008.
 351.Van Wingen GA, Ossewaarde L, Bäckström T, Hermans EJ, Fernández G. Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience 191: 38‐45, 2011.
 352.Wise V, McFarlane AC, Clark CR, Battersby M. An integrative assessment of brain and body function “at rest” in panic disorder: A combined quantitative EEG/autonomic function study. Int J Psychophysiol 79: 155‐165, 2011.
 353.Wisner KL, Sit DY, McShea MC, Rizzo DM, Zoretich RA, Hughes CL, Eng HF, Luther JF, Wisniewski SR, Costantino ML, Confer AL, Moses‐Kolko EL, Famy CS, Hanusa BH. Onset timing, thoughts of self‐harm, and diagnoses in postpartum women with screen‐positive depression findings. JAMA Psychiatry 70: 490‐498, 2013.
 354.Witte MM, Resuehr D, Chandler AR, Mehle AK, Overton JM. Female mice and rats exhibit species‐specific metabolic and behavioral responses to ovariectomy. Gen Comp Endocrinol 166: 520‐528, 2010.
 355.Wolkowitz OM, Reus VI, Keebler A, Nelson N, Friedland M, Brizendine L, Roberts E. Double‐blind treatment of major depression with dehydroepiandrosterone. Am J Psychiatry 156: 646‐649, 1999.
 356.Woolley CS, McEwen BS. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat [published erratum appears in J Neurosci 1992 Oct; 12(10): following table of contents]. J Neurosci 12: 2549‐2554, 1992.
 357.Woolley CS, McEwen BS. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336: 293‐306, 1993.
 358.Woolley CS, McEwen BS. Estradiol regulates hippocampal dendritic spine density via an N‐methyl‐d‐aspartate receptor‐dependent mechanism. J Neurosci 14: 7680‐7687, 1994.
 359.Yaffe K, Ettinger B, Pressman A, Seeley D, Whooley M, Schaefer C, Cummings S. Neuropsychiatric function and dehydroepiandrosterone sulfate in elderly women: A prospective study. Biol Psychiatry 43: 694‐700, 1998.
 360.Yao J, Irwin R, Chen S, Hamilton R, Cadenas E, Brinton RD. Ovarian hormone loss induces bioenergetic deficits and mitochondrial β‐amyloid. Neurobiol Aging 33: 1507‐1521, 2012.
 361.Yen Y‐C, Rebok GW, Gallo JJ, Jones RN, Tennstedt SL. Depressive symptoms impair everyday problem‐solving ability through cognitive abilities in late life. Am J Geriatr Psychiatry 19: 142‐150, 2011.
 362.Zeidan MA, Igoe SA, Linnman C, Vitalo A, Levine JB, Klibanski A, Goldstein JM, Milad MR. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol Psychiatry 70: 920‐927, 2011.
 363.Zhang D, Yang S, Yang C, Jin G, Zhen X. Estrogen regulates responses of dopamine neurons in the ventral tegmental area to cocaine. Psychopharmacology (Berl) 199: 625‐635, 2008.
 364.Zhang L, Li Bs, Zhao W, Chang YH, Ma W, Dragan M, Barker JL, Hu Q, Rubinow DR. Sex‐related differences in MAPKs activation in rat astrocytes: Effects of estrogen on cell death. Brain Res Mol Brain Res 103: 1‐11, 2002.
 365.Zhou Y, Watters JJ, Dorsa DM. Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain. Endocrinology 137: 2163‐2166, 1996.
 366.Zhou Y, Yu C, Zheng H, Liu Y, Song M, Qin W, Li K, Jiang T. Increased neural resources recruitment in the intrinsic organization in major depression. J Affect Disord 121: 220‐230, 2010.

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Crystal Edler Schiller, Sarah L. Johnson, Anna C. Abate, Peter J. Schmidt, David R. Rubinow. Reproductive Steroid Regulation of Mood and Behavior. Compr Physiol 2016, 6: 1135-1160. doi: 10.1002/cphy.c150014