Neuroimaging the Menstrual Cycle and Premenstrual Dysphoric Disorder

Current Psychiatry Reports

Volumn 17, Issue 10, 2015, Pages

  Comasco, Erika ^a,b   Sundström Poromaa, Inger ^b  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Estrogen; fMRI; Menstrual cycle; PET; PMDD; Progesterone; Women

Indexed keywords

ANDROGEN RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CATECHOL METHYLTRANSFERASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GESTAGEN; PROGESTERONE RECEPTOR; SEROTONIN NORADRENALIN REUPTAKE INHIBITOR;

BRAIN BLOOD FLOW; BRAIN CHEMISTRY; BRAIN FUNCTION; COGNITION; DEFAULT MODE NETWORK; DIFFUSION TENSOR IMAGING; ELECTROENCEPHALOGRAM; EMOTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC POLYMORPHISM; GENETICS; GRAY MATTER; HUMAN; MENSTRUAL CYCLE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POSITRON EMISSION TOMOGRAPHY; PREMENSTRUAL DYSPHORIC DISORDER; RESTING STATE FUNCTIONAL MAGNETIC RESONANCE IMAGING; RESTING STATE NETWORK; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; VOXEL BASED MORPHOMETRY; WHITE MATTER; BRAIN; BRAIN MAPPING; FEMALE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SCINTISCANNING;

BRAIN; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MENSTRUAL CYCLE; NEUROIMAGING; POSITRON-EMISSION TOMOGRAPHY; PREMENSTRUAL DYSPHORIC DISORDER;

EID: 84939215915     PISSN: 15233812     EISSN: 15351645     Source Type: Journal    
DOI: 10.1007/s11920-015-0619-4     Document Type: Review

References (107)

1. Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature. 2014;509(7500):282–3.
2. Toffoletto S, Lanzenberger R, Gingnell M, Sundstrom-Poromaa I, Comasco E. Emotional and cognitive functional imaging of estrogen and progesterone effects in the female human brain: a systematic review. Psychoneuroendocrinology. 2014;50:28–52. Comprehensive review of fMRI studies of emotion processing and cognitive functioning in relation to endogenous and exogenous estrogen and progesterone in healthy and premenstrual dysphoric disorder women.
3. Savic I. Sex differences in the human brain, their underpinnings and implications. Progress in Brain Research. Elsevier; 2010.
4. Cahill L. Why sex matters for neuroscience. Nat Rev Neurosci. 2006;7(6):477–84.
5. 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. 2010;62(2):155–98.
6. Sundstrom Poromaa I, Gingnell M. Menstrual cycle influence on cognitive function and emotion processing-from a reproductive perspective. Front Neurosci. 2014;8:380.
7. Cosgrove KP, Mazure CM, Staley JK. Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol Psychiatry. 2007;62(8):847–55.
8. Pletzer B. Sex-specific strategy use and global–local processing: a perspective toward integrating sex differences in cognition. Front Neurosci. 2014;8:425.
9. Wang J, Korczykowski M, Rao H, Fan Y, Pluta J, Gur RC, et al. Gender difference in neural response to psychological stress. Soc Cogn Affect Neurosci. 2007;2(3):227–39.
10. Epperson CN. Premenstrual dysphoric disorder and the brain. Am J Psychiatry. 2013;170(3):248–52.
11. A.P.A. Diagnostic and Statistical Manual of Mental Disorders (5th ed.; DSM-5) 2013.
12. Epperson CN, Steiner M, Hartlage SA, Eriksson E, Schmidt PJ, Jones I, et al. Premenstrual dysphoric disorder: evidence for a new category for DSM-5. Am J Psychiatry. 2012;169(5):465–75.
13. Pearlstein T, Steiner M. Premenstrual dysphoric disorder: burden of illness and treatment update. J Psychiatry Neurosci: JPN. 2008;33(4):291–301.
14. Halbreich U, Borenstein J, Pearlstein T, Kahn LS. The prevalence, impairment, impact, and burden of premenstrual dysphoric disorder (PMS/PMDD). Psychoneuroendocrinology. 2003;28 Suppl 3:1–23.
15. Cunningham J, Yonkers KA, O'Brien S, Eriksson E. Update on research and treatment of premenstrual dysphoric disorder. Harv Rev Psychiatry. 2009;17(2):120–37.
16. Yonkers KA, O'Brien PM, Eriksson E. Premenstrual syndrome. Lancet. 2008;371(9619):1200–10.
17. Wittchen HU, Becker E, Lieb R, Krause P. Prevalence, incidence and stability of premenstrual dysphoric disorder in the community. Psychol Med. 2002;32(1):119–32.
18. Kendler KS, Karkowski LM, Corey LA, Neale MC. Longitudinal population-based twin study of retrospectively reported premenstrual symptoms and lifetime major depression. Am J Psychiatry. 1998;155(9):1234–40.
19. Halbreich U. Selective serotonin reuptake inhibitors and initial oral contraceptives for the treatment of PMDD: effective but not enough. CNS Spectrums. 2008;13(7):566–72.
20. Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, Finch CE, et al. Progesterone receptors: form and function in brain. Front Neuroendocrinol. 2008;29(2):313–39.
21. Arevalo MA, Azcoitia I, Garcia-Segura LM. The neuroprotective actions of oestradiol and oestrogen receptors. Nat Rev Neurosci. 2015;16(1):17–29.
22. Meyer-Lindenberg A, Weinberger DR. Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat Rev Neurosci. 2006;7(10):818–27.
23. Rasetti R, Weinberger DR. Intermediate phenotypes in psychiatric disorders. Curr Opin Gene Dev. 2011;21(3):340–8.
24. Pine DS, Leibenluft E. Biomarkers With a Mechanistic Focus. JAMA Psychiatry. 2015.
25. Friston KJ. Modalities, modes, and models in functional neuroimaging. Science. 2009;326(5951):399–403.
26. Fox PT, Friston KJ. Distributed processing; distributed functions? Neuroimage. 2012;61(2):407–26.
27. Gibbs RB. Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr Rev. 2010;31(2):224–53.
28. Wnuk A, Korol DL, Erickson KI. Estrogens, hormone therapy, and hippocampal volume in postmenopausal women. Maturitas. 2012;73(3):186–90.
29. Voytko ML, Tinkler GP, Browne C, Tobin JR. Neuroprotective effects of estrogen therapy for cognitive and neurobiological profiles of monkey models of menopause. Am J Primatol. 2009;71(9):794–801.
30. Daniel JM. Estrogens, estrogen receptors, and female cognitive aging: the impact of timing. Horm Behav. 2013;63(2):231–7.
31. Lisofsky N, Martensson J, Eckert A, Lindenberger U, Gallinat J, Kuhn S. Hippocampal volume and functional connectivity changes during the female menstrual cycle. NeuroImage. 2015;118:154–62. Multimodal neuroimaging study of healthy women assessed longitudinally four times during the menstrual cycle for grey matter morphometry, white matter organization and functional connectivity.
32. Pletzer B, Kronbichler M, Aichhorn M, Bergmann J, Ladurner G, Kerschbaum HH. Menstrual cycle and hormonal contraceptive use modulate human brain structure. Brain Res. 2010;1348:55–62.
33. Protopopescu X, Butler T, Pan H, Root J, Altemus M, Polanecsky M, et al. Hippocampal structural changes across the menstrual cycle. Hippocampus. 2008;18(10):985–8.
34. Comasco E, Frokjaer VG, Sundstrom-Poromaa I. Functional and molecular neuroimaging of menopause and hormone replacement therapy. Front Neurosci. 2014;8:388.
35. Hagemann G, Ugur T, Schleussner E, Mentzel HJ, Fitzek C, Witte OW, et al. Changes in brain size during the menstrual cycle. PLoS One. 2011;6(2):e14655.
36. Ossewaarde L, van Wingen GA, Rijpkema M, Backstrom T, Hermans EJ, Fernandez G. Menstrual cycle-related changes in amygdala morphology are associated with changes in stress sensitivity. Hum Brain Mapp. 2013;34(5):1187–93.
37. De Bondt T, Jacquemyn Y, Van Hecke W, Sijbers J, Sunaert S, Parizel PM. Regional gray matter volume differences and sex-hormone correlations as a function of menstrual cycle phase and hormonal contraceptives use. Brain Res. 2013;1530:22–31.
38. Petersen N, Touroutoglou A, Andreano JM, Cahill L. Oral contraceptive pill use is associated with localized decreases in cortical thickness. Hum Brain Mapp. 2015;36(7):2644–54.
39. Berman SM, London ED, Morgan M, Rapkin AJ. Elevated gray matter volume of the emotional cerebellum in women with premenstrual dysphoric disorder. J Affect Disord. 2013;146(2):266–71.
40. Jeong HG, Ham BJ, Yeo HB, Jung IK, Joe SH. Gray matter abnormalities in patients with premenstrual dysphoric disorder: an optimized voxel-based morphometry. J Affect Disord. 2012;140(3):260–7.
41. Peper JS, van den Heuvel MP, Mandl RC, Hulshoff Pol HE, van Honk J. Sex steroids and connectivity in the human brain: a review of neuroimaging studies. Psychoneuroendocrinology. 2011;36(8):1101–13.
42. De Bondt T, Van Hecke W, Veraart J, Leemans A, Sijbers J, Sunaert S, et al. Does the use of hormonal contraceptives cause microstructural changes in cerebral white matter? Preliminary results of a DTI and tractography study. Eur Radiol. 2013;23(1):57–64.
43. Reiman EM, Armstrong SM, Matt KS, Mattox JH. The application of positron emission tomography to the study of the normal menstrual cycle. Hum Reprod. 1996;11(12):2799–805.
44. Deco G, Jirsa VK, McIntosh AR. Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat Rev Neurosci. 2011;12(1):43–56.
45. Hjelmervik H, Hausmann M, Osnes B, Westerhausen R, Specht K. Resting states are resting traits--an FMRI study of sex differences and menstrual cycle effects in resting state cognitive control networks. PLoS One. 2014;9(7):e103492.
46. Arelin K, Mueller K, Barth C, Rekkas PV, Kratzsch J, Burmann I et al. Progesterone mediates brain functional connectivity changes during the menstrual cycle - a pilot resting state MRI study. Frontiers in neuroscience. 2015. One-subject study of resting state brain connectivity across the menstrual cycle.
47. Petersen N, Kilpatrick LA, Goharzad A, Cahill L. Oral contraceptive pill use and menstrual cycle phase are associated with altered resting state functional connectivity. NeuroImage. 2014;90:24–32.
48. Sacher J, Okon-Singer H, Villringer A. Evidence from neuroimaging for the role of the menstrual cycle in the interplay of emotion and cognition. Front Hum Neurosci. 2013;7(374):00374.
49. Ochsner KN, Gross JJ. The cognitive control of emotion. Trends Cogn Sci. 2005;9(5):242–9.
50. Amin Z, Epperson CN, Constable RT, Canli T. Effects of estrogen variation on neural correlates of emotional response inhibition. Neuroimage. 2006;32(1):457–64.
51. Weis S, Hausmann M. Sex hormones: modulators of interhemispheric inhibition in the human brain. Neuroscientist. 2010;16(2):132–8.
52. Weis S, Hausmann M, Stoffers B, Sturm W. Dynamic changes in functional cerebral connectivity of spatial cognition during the menstrual cycle. Hum Brain Mapp. 2011;32(10):1544–56.
53. Baller EB, Wei SM, Kohn PD, Rubinow DR, Alarcon G, Schmidt PJ, et al. Abnormalities of dorsolateral prefrontal function in women with premenstrual dysphoric disorder: a multimodal neuroimaging study. Am J Psychiatry. 2013;170(3):305–14. Multimodal PET and fMRI study indicating neural correlates of PMDD diagnosis and symptoms.
54. Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biol Psychiatry. 2003;54(5):504–14.
55. Andreano JM, Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. NeuroImage. 2010;53(4):1286–93.
56. Gingnell M, Morell A, Bannbers E, Wikstrom J, Sundstrom PI. Menstrual cycle effects on amygdala reactivity to emotional stimulation in premenstrual dysphoric disorder. Horm Behav. 2012;62(4):400–6.
57. van Wingen G, van Broekhoven F, Verkes RJ, Petersson KM, Backstrom T, Buitelaar J, et al. How progesterone impairs memory for biologically salient stimuli in healthy young women. J Neurosci. 2007;27(42):11416–23.
58. van Wingen GA, van Broekhoven F, Verkes RJ, Petersson KM, Backstrom T, Buitelaar JK, et al. Progesterone selectively increases amygdala reactivity in women. Mol Psychiatry. 2008;13(3):325–33.
59. Ossewaarde L, Hermans EJ, van Wingen GA, Kooijman SC, Johansson IM, Backstrom T, et al. Neural mechanisms underlying changes in stress-sensitivity across the menstrual cycle. Psychoneuroendocrinology. 2010;35(1):47–55.
60. Gingnell M, Ahlstedt V, Bannbers E, Wikstrom J, Sundstrom-Poromaa I, Fredrikson M. Social stimulation and corticolimbic reactivity in premenstrual dysphoric disorder: a preliminary study. Biol Mood Anxiety Disord. 2014;4(1):3.
61. Menon V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci. 2011;15(10):483–506. A scholar review of functional brain networks: DMN, SN, and CEN.
62. Goldstein JM, Jerram M, Poldrack R, Ahern T, Kennedy DN, Seidman LJ, et al. Hormonal cycle modulates arousal circuitry in women using functional magnetic resonance imaging. J Neurosci. 2005;25(40):9309–16.
63. Landen M, Eriksson E. How does premenstrual dysphoric disorder relate to depression and anxiety disorders? Depress Anxiety. 2003;17(3):122–9.
64. Comasco E, Hahn A, Ganger S, Gingnell M, Bannbers E, Oreland L, et al. Emotional fronto-cingulate cortex activation and brain derived neurotrophic factor polymorphism in premenstrual dysphoric disorder. Human Brain Mapping. 2014;35(9):4450–8. First neuroimaging genetic study of PMDD showing an involvement of BDNF genotype on emotion processing in the anterior cingulate cortex during the luteal phase in PMDD patients.
65. Gingnell M, Bannbers E, Wikstrom J, Fredrikson M, Sundstrom-Poromaa I. Premenstrual dysphoric disorder and prefrontal reactivity during anticipation of emotional stimuli. Eur Neuropsychopharmacol. 2013;17(13):00215.
66. Epperson CN, Pittman B, Czarkowski KA, Stiklus S, Krystal JH, Grillon C. Luteal-phase accentuation of acoustic startle response in women with premenstrual dysphoric disorder. Neuropsychopharmacology. 2007;32(10):2190–8.
67. de Frias CM, Nilsson LG, Herlitz A. Sex differences in cognition are stable over a 10-year period in adulthood and old age. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2006;13(3–4):574–87.
68. Hampson E. Variations in sex-related cognitive abilities across the menstrual cycle. Brain Cogn. 1990;14(1):26–43.
69. Arnold AP. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav. 2009;55(5):570–8.
70. Berenbaum SA, Beltz AM. Sexual differentiation of human behavior: effects of prenatal and pubertal organizational hormones. Front Neuroendocrinol. 2011;32(2):183–200.
71. Shepard RN, Metzler J. Mental rotation of three-dimensional objects. Science. 1971;171(3972):701–3.
72. Thimm M, Weis S, Hausmann M, Sturm W. Menstrual cycle effects on selective attention and its underlying cortical networks. Neuroscience. 2014;258:307–17.
73. 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. 2008;28(50):13401–10.
74. Okon-Singer H, Hendler T, Pessoa L, Shackman AJ. The neurobiology of emotion-cognition interactions: fundamental questions and strategies for future research. Front Hum Neurosci. 2015;9:58.
75. Lam RW, Kennedy SH, Mclntyre RS, Khullar A. Cognitive dysfunction in major depressive disorder: effects on psychosocial functioning and implications for treatment. Can J Psychiatry. 2014;59(12):649–54.
76. Bannbers E, Gingnell M, Engman J, Morell A, Comasco E, Kask K, et al. The effect of premenstrual dysphoric disorder and menstrual cycle phase on brain activity during response inhibition. J Affect Disord. 2012;142(1–3):347–50.
77. Barth C, Villringer A, Sacher J. Sex hormones affect neurotransmitters and shape the adult female brain during hormonal transition periods. Front Neurosci. 2015;9:37.
78. Khayum MA, de Vries EF, Glaudemans AW, Dierckx RA, Doorduin J. In vivo imaging of brain estrogen receptors in rats: a 16alpha-18F-fluoro-17beta-estradiol PET study. J Nuclear Med:Off Publ, Soc Nucl Med. 2014;55(3):481–7. PET tracer for neuroimaging of the estrogen receptor in the brain of rodents, and potentially humans.
79. Takahashi K, Hosoya T, Onoe K, Doi H, Nagata H, Hiramatsu T, et al. 11C-cetrozole: an improved C-11C-methylated PET probe for aromatase imaging in the brain. J Nucl Med: Off Publ, Soc Nucl Med. 2014;55(5):852–7.
80. Biegon A, Alexoff DL, Kim SW, Logan J, Pareto D, Schlyer D, et al. Aromatase imaging with [N-methyl-11C]vorozole PET in healthy men and women. J Nucl Med: Off Publ, Soc Nucl Med. 2015;56(4):580–5.
81. Balthazart J, Ball GF. New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci. 1998;21(6):243–9.
82. Cornil CA. Rapid regulation of brain oestrogen synthesis: the behavioural roles of oestrogens and their fates. J Neuroendocrinol. 2009;21(3):217–26.
83. Roselli CE, Liu M, Hurn PD. Brain aromatization: classic roles and new perspectives. Semin Reprod Med. 2009;27(3):207–17.
84. Harada M, Kubo H, Nose A, Nishitani H, Matsuda T. Measurement of variation in the human cerebral GABA level by in vivo MEGA-editing proton MR spectroscopy using a clinical 3 T instrument and its dependence on brain region and the female menstrual cycle. Hum Brain Mapp. 2011;32(5):828–33.
85. Epperson CN, Haga K, Mason GF, Sellers E, Gueorguieva R, Zhang W, et al. Cortical y-aminobutyric acid levels across the menstrual cycle in healthy women and those with premenstrual dysphoric disorder: A 1H-MRS study. Arch Gene Psychiatry. 2002;59(9):851–8. The first study neuroimaging GABA in relation to the menstrual cycle and PMDD.
86. De Bondt T, De Belder F, Vanhevel F, Jacquemyn Y, Parizel PM. Prefrontal GABA concentration changes in women-Influence of menstrual cycle phase, hormonal contraceptive use, and correlation with premenstrual symptoms. Brain Res. 2015;1597:129–38.
87. Batra NA, Seres-Mailo J, Hanstock C, Seres P, Khudabux J, Bellavance F, et al. Proton magnetic resonance spectroscopy measurement of brain glutamate levels in premenstrual dysphoric disorder. Biol Psychiatry. 2008;63(12):1178–84.
88. Rasgon NL, Thomas MA, Guze BH, Fairbanks LA, Yue K, Curran JG, et al. Menstrual cycle-related brain metabolite changes using 1H magnetic resonance spectroscopy in premenopausal women: a pilot study. Psychiatry Res. 2001;106(1):47–57.
89. Chrzan R, Tomaszuk M, Urbanik A. The influence of the menstrual cycle on the result of brain examination with hydrogen magnetic resonance spectroscopy - a pilot study. Neurol Neurochir Pol. 2013;47(5):450–5.
90. Jovanovic H, Cerin A, Karlsson P, Lundberg J, Halldin C, Nordstrom AL. A PET study of 5-HT1A receptors at different phases of the menstrual cycle in women with premenstrual dysphoria. Psychiatry Res. 2006;148(2–3):185–93.
91. Jovanovic H, Karlsson P, Cerin A, Halldin C, Nordstrom AL. 5-HT(1A) receptor and 5-HTT binding during the menstrual cycle in healthy women examined with [(11)C] WAY100635 and [(11)C] MADAM PET. Psychiatry Res. 2009;172(1):31–7.
92. Moses-Kolko EL, Price JC, Shah N, Berga S, Sereika SM, Fisher PM, et al. Age, sex, and reproductive hormone effects on brain serotonin-1A and serotonin-2A receptor binding in a healthy population. Neuropsychopharmacology. 2011;36(13):2729–40.
93. Nordstrom AL, Olsson H, Halldin C. A PET study of D2 dopamine receptor density at different phases of the menstrual cycle. Psychiatry Res. 1998;83(1):1–6.
94. Eriksson O, Wall A, Marteinsdottir I, Agren H, Hartvig P, Blomqvist G, et al. Mood changes correlate to changes in brain serotonin precursor trapping in women with premenstrual dysphoria. Psychiatry Res. 2006;146(2):107–16.
95. Liu B, Wang G, Gao D, Gao F, Zhao B, Qiao M, et al. Alterations of GABA and glutamate-glutamine levels in premenstrual dysphoric disorder: a 3T proton magnetic resonance spectroscopy study. Psychiatry Res. 2015;231(1):64–70.
96. Jacobs E, D'Esposito M. Estrogen shapes dopamine-dependent cognitive processes: implications for women's health. J Neurosci. 2011;31(14):5286–93.
97. Bath KG, Chuang J, Spencer-Segal JL, Amso D, Altemus M, McEwen BS, et al. Variant brain-derived neurotrophic factor (Valine66Methionine) polymorphism contributes to developmental and estrous stage-specific expression of anxiety-like behavior in female mice. Biol Psychiatry. 2012;72(6):499–504.
98. Brown J, O' Brien PM, Marjoribanks J, Wyatt K. Selective serotonin reuptake inhibitors for premenstrual syndrome. Cochrane Database Syst Rev. 2009;2:CD001396.
99. Nordquist N, Oreland L. Serotonin, genetic variability, behaviour, and psychiatric disorders—a review. Ups J Med Sci. 2010;115(1):2–10.
100. Sundstrom-Poromaa I, Bixo M, Bjorn I, Nordh O. Compliance to antidepressant drug therapy for treatment of premenstrual syndrome. J Psychosom Obstet Gynaecol. 2000;21(4):205–11.
101. Wyatt KM, Dimmock PW, Ismail KM, Jones PW, O'Brien PM. The effectiveness of GnRHa with and without 'add-back' therapy in treating premenstrual syndrome: a meta analysis. BJOG. 2004;111(6):585–93.
102. Segebladh B, Borgstrom A, Nyberg S, Bixo M, Sundstrom-Poromaa I. Evaluation of different add-back estradiol and progesterone treatments to gonadotropin-releasing hormone agonist treatment in patients with premenstrual dysphoric disorder. Am J Obstet Gynecol. 2009;201(2):1–8.
103. Andreen L, Bixo M, Nyberg S, Sundstrom-Poromaa I, Backstrom T. Progesterone effects during sequential hormone replacement therapy. Eur J Endocrinol. 2003;148(5):571–7.
104. Andreen L, Sundstrom-Poromaa I, Bixo M, Andersson A, Nyberg S, Backstrom T. Relationship between allopregnanolone and negative mood in postmenopausal women taking sequential hormone replacement therapy with vaginal progesterone. Psychoneuroendocrinology. 2005;30(2):212–24.
105. Andreen L, Sundstrom-Poromaa I, Bixo M, Nyberg S, Backstrom T. Allopregnanolone concentration and mood—a bimodal association in postmenopausal women treated with oral progesterone. Psychopharmacology (Berl). 2006;187(2):209–21.
106. Baroncini M, Jissendi P, Catteau-Jonard S, Dewailly D, Pruvo JP, Francke JP, et al. Sex steroid hormones-related structural plasticity in the human hypothalamus. NeuroImage. 2010;50(2):428–33.
107. Henderson VW, Greicius MD. Functional magnetic resonance imaging and estrogen effects on the brain: cautious interpretation of a BOLD finding. Menopause. 2010;17(4):669–71.