Using position emission tomography to investigate hormone-mediated neurochemical changes across the female lifespan: implications for depression

International Review of Psychiatry

Volumn 29, Issue 6, 2017, Pages 580-596

  Zsido, Rachel G ^a   Villringer, Arno ^a,b   Sacher, Julia ^a,b  

^a MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Estrogen; mood disorders; perimenopause; positron emission tomography; post partum; pre menstrual dysphoric disorder; progesterone; sex differences

Indexed keywords

ESTROGEN; PROGESTERONE;

CLIMACTERIUM; CLINICAL RESEARCH; DEPRESSION; HORMONE ACTION; HUMAN; LIFESPAN; MENSTRUAL CYCLE; MONOAMINERGIC SYSTEM; NEUROCHEMISTRY; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PUERPERIUM; REVIEW; SEX DIFFERENCE; VULNERABLE POPULATION; BRAIN; METABOLISM; PROCEDURES; PSYCHOLOGY; SEX FACTOR;

BRAIN; DEPRESSION; ESTROGENS; HUMANS; NEUROCHEMISTRY; PERIMENOPAUSE; POSITRON-EMISSION TOMOGRAPHY; POSTPARTUM PERIOD; PROGESTERONE; SEX FACTORS;

EID: 85038236618     PISSN: 09540261     EISSN: 13691627     Source Type: Journal    
DOI: 10.1080/09540261.2017.1397607     Document Type: Review

References (116)

1. Adams, M.M., Fink, S.E., Janssen, W.G., Shah, R.A., & Morrison, J.H., (2004). Estrogen modulates synaptic N‐methyl‐D‐aspartate receptor subunit distribution in the aged hippocampus. Journal of Comparative Neurology, 474, 419–426.doi:10.1002/cne.20148
2. Aiello, M., Salvatore, E., Cachia, A., Pappatà, S., Cavaliere, C., Prinster, A., … Quarantelli, M., (2015). Relationship between simultaneously acquired resting-state regional cerebral glucose metabolism and functional MRI: A PET/MR hybrid scanner study. Neuroimage, 113, 111–121. doi:10.1016/j.neuroimage.2015.03.017
3. Angst, J., & Dobler-Mikola, A., (1984). Do the diagnostic criteria determine the sex ratio in depression? Journal of Affective Disorders, 7, 189–198.doi:10.1016/0165-0327(84)90040-5
4. Antunes, I.F., van Waarde, A., Dierckx, R.A., de Vries, E.G., Hospers, G.A., & de Vries, E.F., (2017). Synthesis and evaluation of the estrogen receptor β–selective radioligand 2-18F-fluoro-6-(6-Hydroxynaphthalen-2-yl) pyridin-3-ol: Comparison with 16α-18F-Fluoro-17β-Estradiol. Journal of Nuclear Medicine, 58, 554–559. doi:10.2967/jnumed.116.180158
5. Antunes, I.F., Willemsen, A.T., Sijbesma, J.W., Boerema, A.S., van Waarde, A., Glaudemans, A.W., … de Vries, E.F., (2017). In vivo quantification of ER-β expression by pharmacokinetic modeling: Studies with 18F-FHNP PET. Journal of Nuclear Medicine, 58, 1743–1748. doi:10.2967/jnumed.117.192666
6. Arélin, K., Mueller, K., Barth, C., Rekkas, P.V., Kratzsch, J., Burmann, I., … Sacher, J. (2015). Progesterone mediates brain functional connectivity changes during the menstrual cycle: A pilot resting state MRI study. Frontiers in Neuroscience, 9, 44. doi:10.3389/fnins.2015.00044
7. Atzil, S., Touroutoglou, A., Rudy, T., Salcedo, S., Feldman, R., Hooker, J.M., … Barrett, L.F., (2017). Dopamine in the medial amygdala network mediates human bonding. Proceedings of the National Academy of Sciences, 114, 2361–2366. doi:10.1073/pnas.1612233114
8. Bäckström, T., Andreen, L., Birzniece, V., Björn, I., Johansson, I.M., Nordenstam-Haghjo, M., … Zhu, D., (2003). The role of hormones and hormonal treatments in premenstrual syndrome. CNS Drugs, 17, 325–342. doi:10.2165/00023210-200317050-00003
9. Bäckström, T., Bixo, M., Johansson, M., Nyberg, S., Ossewaarde, L., Ragagnin, G., … van Wingen, G., (2014). Allopregnanolone and mood disorders. Progress in Neurobiology, 113, 88–94. doi:10.1016/j.pneurobio.2013.07.005
10. Barth, C., Steele, C.J., Mueller, K., Rekkas, V.P., Arélin, K., Pampel, A., … Sacher, J., (2016). In-vivo dynamics of the human hippocampus across the menstrual cycle. Scientific Reports, 6. doi:10.1038/srep32833
11. Barth, C., Villringer, A., & Sacher, J., (2015). Sex hormones affect neurotransmitters and shape the adult female brain during hormonal transition periods. Frontiers in Neuroscience, 9. doi:10.3389/fnins.2015.00037
12. Baxter, L.R., Phelps, M.E., Mazziotta, J.C., Schwartz, J.M., Gerner, R.H., Selin, C.E., & Sumida, R.M., (1985). Cerebral metabolic rates for glucose in mood disorders: Studies with positron emission tomography and fluorodeoxyglucose F 18. Archives of General Psychiatry, 42, 441–447.doi:10.1001/archpsyc.1985.01790280019002
13. Baxter, L.R., Schwartz, J.M., Phelps, M.E., Mazziotta, J.C., Guze, B.H., Selin, C.E., … Sumida, R.M., (1989). Reduction of prefrontal cortex glucose metabolism common to three types of depression. Archives of General Psychiatry, 46, 243–250. doi:10.1001/archpsyc.1989.01810030049007
14. Bench, C.J., Friston, K.J., Brown, R.G., Frackowiak, R.S.J., & Dolan, R.J., (1993). Regional cerebral blood flow in depression measured by positron emission tomography: the relationship with clinical dimensions. Psychological Medicine, 23, 579–590.doi:10.1017/S0033291700025368
15. Bethea, C.L., Mirkes, S.J., Shively, C.A., & Adams, M.R., (2000). Steroid regulation of tryptophan hydroxylase protein in the dorsal raphe of macaques. Biological Psychiatry, 47, 562–576.doi:10.1016/S0006-3223(99)00156-0
16. Biegon, A., Alexoff, D.L., Kim, S.W., Logan, J., Pareto, D., Schlyer, D., … Fowler, J.S., (2015). Aromatase imaging with [N-methyl-11C] vorozole PET in healthy men and women. Journal of Nuclear Medicine, 56, 580–585. doi:10.2967/jnumed.114.150383
17. Brooks, J.O., Wang, P.W., Bonner, J.C., Rosen, A.C., Hoblyn, J.C., Hill, S.J., & Ketter, T.A., (2009). Decreased prefrontal, anterior cingulate, insula, and ventral striatal metabolism in medication-free depressed outpatients with bipolar disorder. Journal of Psychiatric Research, 43, 181–188. doi:10.1016/j.jpsychires.2008.04.015
18. Buchsbaum, M.S., Joseph, W., Siegel, B.V., Hackett, E., Trenary, M., Abel, L., & Reynolds, C., (1997). Effect of sertraline on regional metabolic rate in patients with affective disorder. Biological Psychiatry, 41, 15–22.doi:10.1016/S0006-3223(96)00097-2
19. Cahill, L., Haier, R.J., White, N.S., Fallon, J., Kilpatrick, L., Lawrence, C., … Alkire, M.T., (2001). Sex-related difference in amygdala activity during emotionally influenced memory storage. Neurobiology of Learning and Memory, 75, 1–9. doi:10.1006/nlme.2000.3999
20. Chen, Q., Liu, W., Li, H., Zhang, H., & Tian, M., (2011). Molecular imaging in patients with mood disorders: a review of PET findings. European Journal of Nuclear Medicine and Molecular Imaging, 38, 1367–1380.doi:10.1007/s00259-011-1779-z
21. Costes, N., Merlet, I., Ostrowsky, K., Faillenot, I., Lavenne, F., Zimmer, L., … Le Bars, D., (2005). A 18F-MPPF PET normative database of 5-HT1A receptor binding in men and women over aging. Journal of Nuclear Medicine, 46, 1980–1989.Retrieved from http://jnm.snmjournals.org/content/46/12/1980.full
22. Cuthbert, B.N., (2014). The RDoC framework: Facilitating transition from ICD/DSM to dimensional approaches that integrate neuroscience and psychopathology. World Psychiatry, 13, 28–35. Retrieved from http://doi.org/10.1002/wps.20087
23. Deecher, D., Andree, T.H., Sloan, D., & Schechter, L.E., (2008). From menarche to menopause: Exploring the underlying biology of depression in women experiencing hormonal changes. Psychoneuroendocrinology, 33, 3–17.doi:10.1016/j.psyneuen.2007.10.006
24. Delgado, P.L., (2000). Depression: The case for a monoamine deficiency. The Journal of Clinical Psychiatry, 61(Suppl 6), 7–11.Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/10775018
25. Di Paolo, T., Falardeau, P., & Morissette, M., (1988). Striatal D-2 dopamine agonist binding sites fluctuate during the rat estrous cycle. Life Sciences, 43, 665–672.doi:10.1016/0024-3205(88)90137-3
26. Dowlati, Y., Ravindran, A.V., Segal, Z.V., Stewart, D.E., Steiner, M., & Meyer, J.H., (2017). Selective dietary supplementation in early postpartum is associated with high resilience against depressed mood. Proceedings of the National Academy of Sciences, 114, 3509–3514.doi:10.1073/pnas.1611965114
27. Drevets, W.C., Gautier, C., Price, J.C., Kupfer, D.J., Kinahan, P.E., Grace, A.A., … Mathis, C.A., (2001). Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biological Psychiatry, 49, 81–96. doi:10.1016/S0006-3223(00)01038-6
28. Drevets, W.C., Price, J.L., Bardgett, M.E., Reich, T., Todd, R.D., & Raichle, M.E., (2002). Glucose metabolism in the amygdala in depression: Relationship to diagnostic subtype and plasma cortisol levels. Pharmacology Biochemistry and Behavior, 71, 431–447.doi:10.1016/S0091-3057(01)00687-6
29. Drevets, W.C., Price, J.L., Simpson, J.R., Jr., Todd, R.D., Reich, T., Vannier, M., & Raichle, M.E., (1997). Subgenual prefrontal cortex abnormalities in mood disorders. Nature, 386, 824. doi:10.1038/386824a0
30. Dunlop, B.W., & Nemeroff, C.B., (2007). The role of dopamine in the pathophysiology of depression. Archives of general psychiatry, 64, 327–337.doi:10.1001/archpsyc.64.3.327
31. Eriksson, O., Wall, A., Marteinsdottir, I., Ågren, H., Hartvig, P., Blomqvist, G., … Naessén, T., (2006). Mood changes correlate to changes in brain serotonin precursor trapping in women with premenstrual dysphoria. Psychiatry Research: Neuroimaging, 146, 107–116. doi:10.1016/j.pscychresns.2005.02.012
32. FitzGerald, M., Malone, K.M., Li, S., Harrison, W.M., McBride, P.A., Endicott, J., … Mann, J.J., (1997). Blunted serotonin response to fenfluramine challenge in premenstrual dysphoric disorder. American Journal of Psychiatry, 154, 556–558. doi:10.1176/ajp.154.4.556
33. Frank, E., Carpenter, L.L., & Kupfer, D.J., (1988). Sex differences in recurrent depression: are there any that are significant?. The American Journal of Psychiatry, 145, 41. doi:10.1176/ajp.145.1.41
34. Freeman, E.W., Sammel, M.D., Boorman, D.W., & Zhang, R., (2014). Longitudinal pattern of depressive symptoms around natural menopause. JAMA Psychiatry, 71, 36–43.doi:10.1001/jamapsychiatry.2013.2819
35. Freeman, E.W., Sammel, M.D., Lin, H., & Nelson, D.B., (2006). Associations of hormones and menopausal status with depressed mood in women with no history of depression. Archives of General Psychiatry, 63, 375–382.doi:10.1001/archpsyc.63.4.375
36. Frey, B.N., Skelin, I., Sakai, Y., Nishikawa, M., & Diksic, M., (2010). Gender differences in α-[11 C] MTrp brain trapping, an index of serotonin synthesis, in medication-free individuals with major depressive disorder: A positron emission tomography study. Psychiatry Research: Neuroimaging, 183, 157–166. doi:10.1016/j.pscychresns.2010.05.005
37. Frokjaer, V.G., Pinborg, A., Holst, K.K., Overgaard, A., Henningsson, S., Heede, M., … Stenbaek, D.S., (2015). Role of serotonin transporter changes in depressive responses to sex-steroid hormone manipulation: A positron emission tomography study. Biological Psychiatry, 78, 534–543. doi:10.1016/j.biopsych.2015.04.015
38. Gavin, N.I., Gaynes, B.N., Lohr, K.N., Meltzer-Brody, S., Gartlehner, G., & Swinson, T., (2005). Perinatal depression: a systematic review of prevalence and incidence. Obstetrics & Gynecology, 106, 1071–1083.doi:10.1097/01.AOG.0000183597.31630.db
39. Gazzaley, A.H., Weiland, N.G., McEwen, B.S., & Morrison, J.H., (1996). Differential regulation of NMDAR1 mRNA and protein by estradiol in the rat hippocampus. Journal of Neuroscience, 16, 6830–6838. Retrieved from http://www.jneurosci.org/content/16/21/6830.short
40. Gundlah, C., Lu, N.Z., & Bethea, C.L., (2002). Ovarian steroid regulation of monoamine oxidase-A and -B mRNAs in the macaque dorsal raphe and hypothalamic nuclei. Psychopharmacology (Berlin), 160, 271–282.doi:10.1007/s00213-001-0959-0
41. Hasler, G., Fromm, S., Carlson, P.J., Luckenbaugh, D.A., Waldeck, T., Geraci, M., … Drevets, W.C., (2008). Neural response to catecholamine depletion in unmedicated subjects with major depressive disorder in remission and healthy subjects. Archives of General Psychiatry, 65, 521–531. doi:10.1001/archpsyc.65.5.521
42. Hausmann, M., & Güntürkün, O., (2000). Steroid fluctuations modify functional cerebral asymmetries: The hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia, 38, 1362–1374. doi:10.1016/S0028-3932(00)00045-2
43. Henderson, J.A., & Bethea, C.L., (2008). Differential effects of ovarian steroids and raloxifene on serotonin 1A and 2C receptor protein expression in macaques. Endocrine, 33, 285–293.doi:10.1007/s12020-008-9087-5
44. Hosokawa, T., Momose, T., & Kasai, K., (2009). Brain glucose metabolism difference between bipolar and unipolar mood disorders in depressed and euthymic states. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 33, 243–250.doi:10.1016/j.pnpbp.2008.11.014
45. Jacobs, E., & D’esposito, M., (2011). Estrogen shapes dopamine-dependent cognitive processes: Implications for women’s health. Journal of Neuroscience, 31, 5286–5293. doi:10.1523/JNEUROSCI.6394-10.2011
46. Jovanovic, H., Cerin, Å., Karlsson, P., Lundberg, J., Halldin, C., & Nordström, A.L., (2006). A PET study of 5-HT 1A receptors at different phases of the menstrual cycle in women with premenstrual dysphoria. Psychiatry Research: Neuroimaging, 148, 185–193. doi:10.1016/j.pscychresns.2006.05.002
47. Jovanovic, H., Karlsson, P., Cerin, Å., Halldin, C., & Nordström, A.L., (2009). 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 Research: Neuroimaging, 172, 31–37. doi:10.1016/j.pscychresns.2008.07.002
48. Jovanovic, H., Lundberg, J., Karlsson, P., Cerin, Å., Saijo, T., Varrone, A., … Nordström, A.L., (2008). Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. Neuroimage, 39, 1408–1419. doi:10.1016/j.neuroimage.2007.10.016
49. Kennedy, S.H., Evans, K.R., Krüger, S., Mayberg, H.S., Meyer, J.H., McCann, S., … Vaccarino, F.J., (2001). Changes in regional brain glucose metabolism measured with positron emission tomography after paroxetine treatment of major depression. American Journal of Psychiatry, 158, 899–905. doi:10.1176/appi.ajp.158.6.899
50. Kessler, R.C., (2003). Epidemiology of women and depression. Journal of Affective Disorders, 74, 5–13.doi:10.1016/S0165-0327(02)00426-3
51. Kessler, R.C., McGonagle, K.A., Zhao, S., Nelson, C.B., Hughes, M., Eshleman, S., … Kendler, K.S., (1994). Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States: results from the National Comorbidity Survey. Archives of General Psychiatry, 51, 8–19. doi:10.1001/archpsyc.1994.03950010008002
52. Ketter, T.A., Kimbrell, T.A., George, M.S., Dunn, R.T., Speer, A.M., Benson, B.E., … Post, R.M., (2001). Effects of mood and subtype on cerebral glucose metabolism in treatment-resistant bipolar disorder. Biological Psychiatry, 49, 97–109. doi:10.1016/S0006-3223(00)00975-6
53. Kimbrell, T.A., Ketter, T.A., George, M.S., Little, J.T., Benson, B.E., Willis, M.W., … Post, R.M., (2002). Regional cerebral glucose utilization in patients with a range of severities of unipolar depression. Biological Psychiatry, 51, 237–252. doi:10.1016/S0006-3223(01)01216-1
54. Konarski, J.Z., McIntyre, R.S., Soczynska, J.K., Bottas, A., & Kennedy, S.H., (2006). Clinical translation of neuroimaging research in mood disorders. Psychiatry (Edgmont), 3, 46. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2990553/
55. Koob, G.F., Everitt, B.J., & Robbins, T.W., (2013). Reward, motivation, and addiction. In Fundamental Neuroscience. 3rd ed. Amsterdam: Academic Press; 987–1016.
56. Kornstein, S.G., Schatzberg, A.F., Thase, M.E., Yonkers, K.A., McCullough, J.P., Keitner, G.I., … Davis, S.M., (2000). Gender differences in chronic major and double depression. Journal of Affective Disorders, 60, 1–11. doi:10.1016/S0165-0327(99)00158-5
57. Laakso, A., Vilkman, H., Örgen Bergman, J., Haaparanta, M., Solin, O., Syvälahti, E., … Hietala, J., (2002). Sex differences in striatal presynaptic dopamine synthesis capacity in healthy subjects. Biological Psychiatry, 52, 759–763. doi:10.1016/S0006-3223(02)01369-0
58. Le Strat, Y., Dubertret, C., & Le Foll, B., (2011). Prevalence and correlates of major depressive episode in pregnant and postpartum women in the United States. Journal of Affective Disorders, 135, 128–138.doi:10.1016/j.jad.2011.07.004
59. Lévesque, D., Gagnon, S., & Di Paolo, T., (1989). Striatal D 1 dopamine receptor density fluctuates during the rat estrous cycle. Neuroscience Letters, 98, 345–350. doi:10.1016/0304-3940(89)90426-6
60. Lin, F.I., Gonzalez, E.M., Kummar, S., Do, K., Shih, J., Adler, S., … Bhattacharyya, S., (2017). Utility of 18F-fluoroestradiol (18F-FES) PET/CT imaging as a pharmacodynamic marker in patients with refractory estrogen receptor-positive solid tumors receiving Z-endoxifen therapy. European Journal of Nuclear Medicine and Molecular Imaging, 44, 500–508. doi:10.1007/s00259-016-3561-8
61. Lisofsky, N., Mårtensson, J., Eckert, A., Lindenberger, U., Gallinat, J., & Kühn, S., (2015). Hippocampal volume and functional connectivity changes during the female menstrual cycle. Neuroimage, 118, 154–162. doi:10.1016/j.neuroimage.2015.06.012
62. Lu, N.Z., & Bethea, C.L., (2002). Ovarian steroid regulation of 5-HT1A receptor binding and G protein activation in female monkeys. Neuropsychopharmacology, 27, 12–24.doi:10.1016/S0893-133X(01)00423-7
63. Mehta, D., Newport, D.J., Frishman, G., Kraus, L., Rex-Haffner, M., Ritchie, J.C., … Stowe, Z.N., (2014). Early predictive biomarkers for postpartum depression point to a role for estrogen receptor signaling. Psychological Medicine, 44, 2309–2322. doi:10.1017/S0033291713003231
64. Meltzer, C.C., Drevets, W.C., Price, J.C., Mathis, C.A., Lopresti, B., Greer, P.J., … Reynolds, C.F., (2001). Gender-specific aging effects on the serotonin 1A receptor. Brain Research, 895, 9–17. doi:10.1016/S0006-8993(00)03211-X
65. Meyer, J.H., Ginovart, N., Boovariwala, A., Sagrati, S., Hussey, D., Garcia, A., … Houle, S., (2006). Elevated monoamine oxidase a levels in the brain: An explanation for the monoamine imbalance of major depression. Archives of General Psychiatry, 63, 1209–1216. doi:10.1001/archpsyc.63.11.1209
66. Meyer, J.H., Houle, S., Sagrati, S., Carella, A., Hussey, D.F., Ginovart, N., … Wilson, A.A., (2004). Brain serotonin transporter binding potential measured with carbon 11–labeled DASB positron emission tomography: Effects of major depressive episodes and severity of dysfunctional attitudes. Archives of General Psychiatry, 61, 1271–1279. doi:10.1001/archpsyc.61.12.1271
67. Meyer, J.H., Wilson, A.A., Sagrati, S., Miler, L., Rusjan, P., Bloomfield, P.M., … Houle, S., (2009). Brain monoamine oxidase A binding in major depressive disorder: Relationship to selective serotonin reuptake inhibitor treatment, recovery, and recurrence. Archives of General Psychiatry, 66, 1304–1312. doi:10.1001/archgenpsychiatry.2009.156
68. Mitchell, E.S., Woods, N.F., & Mariella, A., (2000). Three stages of the menopausal transition from the Seattle Midlife Women’s Health Study: Toward a more precise definition. Menopause, 7, 334–349. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/10993033
69. Moreno, F.A., McGahuey, C.A., Freeman, M.P., & Delgado, P.L., (2006). Sex differences in depressive response during monoamine depletions in remitted depressive subjects. The Journal of Clinical Psychiatry, 67, 1618–1623.doi:10.4088/JCP.v67n1019
70. Moses-Kolko, E.L., Price, J.C., Wisner, K.L., Hanusa, B.H., Meltzer, C.C., Berga, S.L., … Drevets, W.C., (2012). Postpartum and depression status are associated with lower [11C] raclopride BPND in reproductive-age women. Neuropsychopharmacology, 37, 1422. doi:10.1038/npp.2011.328
71. Moses-Kolko, E.L., Wisner, K.L., di Scalea, T.L., Kaye, W.H., Price, J.C., Grace, A.A., … Becker, C., (2006). Reduced ventral striatal D2/D3 receptor binding in depressed reproductive-aged women: A [C-11] raclopride positron emission tomography study. In Neuropsychopharmacology (Vol.31, pp. S87–S88). London, UK: Nature Publishing Group.
72. Moses-Kolko, E.L., Wisner, K.L., Price, J.C., Berga, S.L., Drevets, W.C., Hanusa, B.H., … Meltzer, C.C., (2008). Serotonin 1A receptor reductions in postpartum depression: A positron emission tomography study. Fertility and Sterility, 89, 685–692. doi:10.1016/j.fertnstert.2007.03.059
73. Munro, C.A., McCaul, M.E., Wong, D.F., Oswald, L.M., Zhou, Y., Brasic, J., … Wand, G.S., (2006). Sex differences in striatal dopamine release in healthy adults. Biological Psychiatry, 59, 966–974. doi:10.1016/j.biopsych.2006.01.008
74. Murphy, D.D., Cole, N.B., Greenberger, V., & Segal, M., (1998). Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. Journal of Neuroscience, 18, 2550–2559. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/9502814
75. National Institutes of Health. (2015). Consideration of Sex as a Biological Variable in NIH-funded Research. Retrieved from https://grants.nih.gov/grants/guide/notice-files/NOT-OD-15-102.html
76. Nestler, E.J., & Carlezon, W.A., (2006). The mesolimbic dopamine reward circuit in depression. Biological Psychiatry, 59, 1151–1159.doi:10.1016/j.biopsych.2005.09.018
77. Nishizawa, S., Benkelfat, C., Young, S.N., Leyton, M., Mzengeza, S.D., De Montigny, C., … Diksic, M., (1997). Differences between males and females in rates of serotonin synthesis in human brain. Proceedings of the National Academy of Sciences, 94, 5308–5313. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC24674/
78. O’hara, M.W., Stuart, S., Gorman, L.L., & Wenzel, A., (2000). Efficacy of interpersonal psychotherapy for postpartum depression. Archives of General Psychiatry, 57, 1039–1045. doi:10.1001/archpsyc.57.11.1039
79. O’Higgins, M., Roberts, I.S.J., Glover, V., & Taylor, A., (2013). Mother-child bonding at 1 year; associations with symptoms of postnatal depression and bonding in the first few weeks. Archives of Women’s Mental Health, 16, 381–389. doi:10.1007/s00737-013-0354-y
80. Pareto, D., Biegon, A., Alexoff, D., Carter, P., Shea, C., Muench, L., … Logan, J., (2013). In vivo imaging of brain aromatase in female baboons: [11C] vorozole kinetics and effect of the menstrual cycle. Molecular Imaging, 12, 7290–2013. doi:10.2310/7290.2013.00068
81. Parsey, R.V., Olvet, D.M., Oquendo, M.A., Yung-Yu, H., Ogden, R.T., & Mann, J.J., (2006). Higher 5-HT1A receptor binding potential during a major depressive episode predicts poor treatment response: Preliminary data from a naturalistic study. Neuropsychopharmacology, 31, 1745. doi:10.1038/sj.npp.1300992
82. Parsey, R.V., Oquendo, M.A., Ogden, R.T., Olvet, D.M., Simpson, N., Huang, Y.Y., … Mann, J.J., (2006). Altered serotonin 1A binding in major depression: a [carbonyl-C-11] WAY100635 positron emission tomography study. Biological Psychiatry, 59, 106–113. doi:10.1016/j.biopsych.2005.06.016
83. Parsey, R.V., Oquendo, M.A., Simpson, N.R., Ogden, R.T., Van Heertum, R., Arango, V., & Mann, J.J., (2002). Effects of sex, age, and aggressive traits in man on brain serotonin 5-HT 1A receptor binding potential measured by PET using [C-11] WAY-100635. Brain Research, 954, 173–182.doi:10.1016/S0006-8993(02)03243-2
84. Poobalan, A.S., Aucott, L.S., Ross, L., Smith, W.C.S., Helms, P.J., & Williams, J.H., (2007). Effects of treating postnatal depression on mother–infant interaction and child development. The British Journal of Psychiatry, 191, 378–386.doi:10.1192/bjp.bp.106.032789
85. Rekkas, P.V., Wilson, A.A., Lee, V.W.H., Yogalingam, P., Sacher, J., Rusjan, P., … Chiuccariello, L., (2014). Greater monoamine oxidase A binding in perimenopausal age as measured with carbon 11–labeled harmine positron emission tomography. JAMA Psychiatry, 71, 873–879. doi:10.1001/jamapsychiatry.2014.250
86. Rosa-Neto, P., Diksic, M., Okazawa, H., Leyton, M., Ghadirian, N., Mzengeza, S., … Benkelfat, C., (2004). Measurement of brain regional α-[11C] Methyl-L-tryptophan trapping as a measure of serotonin synthesis in medication-freepatients with major depression. Archives of General Psychiatry, 61, 556–563. doi:10.1001/archpsyc.61.6.556
87. Sabri, O., Seibyl, J., Rowe, C., & Barthel, H., (2015). Beta-amyloid imaging with florbetaben. Clinical and translational imaging, 3, 13–26. doi:10.2967/jnumed.117.193649
88. Sacher, J., Rekkas, P.V., Wilson, A.A., Houle, S., Romano, L., Hamidi, J., … Meyer, J.H., (2015). Relationship of monoamine oxidase-A distribution volume to postpartum depression and postpartum crying. Neuropsychopharmacology, 40, 429. doi:10.1038/npp.2014.190
89. Sacher, J., Wilson, A.A., Houle, S., Rusjan, P., Hassan, S., Bloomfield, P.M., … Meyer, J.H., (2010). Elevated brain monoamine oxidase A binding in the early postpartum period. Archives of General Psychiatry, 67, 468–474. doi:10.1001/archgenpsychiatry.2010.32
90. Sakai, Y., Nishikawa, M., Leyton, M., Benkelfat, C., Young, S.N., & Diksic, M., (2006). Cortical trapping of α-[11 C] methyl-L-tryptophan, an index of serotonin synthesis, is lower in females than males. Neuroimage, 33, 815–824. doi:10.1016/j.neuroimage.2006.08.004
91. Serafini, G., (2012). Neuroplasticity and major depression, the role of modern antidepressant drugs. World Journal of Psychiatry, 2, 49. doi:10.5498/wjp.v2.i3.49
92. Shimizu, H., & Bray, G.A., (1993). Effects of castration, estrogen replacement and estrus cycle on monoamine metabolism in the nucleus accumbens, measured by microdialysis. Brain Research, 621, 200–206.doi:10.1016/0006-8993(93)90107-X
93. Sit, D.K., & Wisner, K.L., (2009). The identification of postpartum depression. Clinical obstetrics and gynecology, 52, 456. doi:10.1097/GRF.0b013e3181b5a57c
94. Skovlund, C.W., Mørch, L.S., & Lidegaard, Ø., (2017). Hormonal contraception and its association with Depression-Reply. Jama Psychiatry, 74, 302–303. doi:10.1001/jamapsychiatry.2016.3865
95. Smith, S.S., & Woolley, C.S., (2004). Cellular and molecular effects of steroid hormones on CNS excitability. Cleveland Clinic Journal of Medicine, 71, S4. doi:10.3949/ccjm.71.Suppl_2.S4
96. Soares, C.N., & Zitek, B., (2008). Reproductive hormone sensitivity and risk for depression across the female life cycle: A continuum of vulnerability?. Journal of Psychiatry & Neuroscience: JPN, 33, 331. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2440795/
97. Sohr-Preston, S.L., & Scaramella, L.V., (2006). Implications of timing of maternal depressive symptoms for early cognitive and language development. Clinical Child and Family Psychology Review, 9, 65–83.doi:10.1007/s10567-006-0004-2
98. Staley, J.K., Krishnan-Sarin, S., Zoghbi, S., Tamagnan, G., Fujita, M., … Innis, R.B., (2001). Sex differences in [123I] β‐CIT SPECT measures of dopamine and serotonin transporter availability in healthy smokers and nonsmokers. Synapse, 41, 275–284. doi:10.1002/syn.1084
99. Stewart, J.L., & Paulus, M.P., (2013). Neural correlates of craving for psychoactive drugs. Principles of Addiction: Comprehensive Addictive Behaviors and Disorders, 1, 453.
100. Su, T.P., Schmidt, P.J., Danaceau, M., Murphy, D.L., & Rubinow, D.R., (1997). Effect of menstrual cycle phase on neuroendocrine and behavioral responses to the serotonin agonist m-chlorophenylpiperazine in women with premenstrual syndrome and controls. The Journal of Clinical Endocrinology & Metabolism, 82, 1220–1228.doi:10.1210/jc.82.4.1220
101. Takahashi, K., Hosoya, T., Onoe, K., Doi, H., Nagata, H., Hiramatsu, T., … Suzuki, M., (2014). 11C-cetrozole: An improved C-11C-methylated PET probe for aromatase imaging in the brain. Journal of Nuclear Medicine, 55, 852–857. doi:10.2967/jnumed.113.131474
102. Van Wingen, G.A., Van Broekhoven, F., Verkes, R.J., Petersson, K.M., Bäckström, T., Buitelaar, J.K., & Fernandez, G., (2008). Progesterone selectively increases amygdala reactivity in women. Molecular Psychiatry, 13, 325. doi:10.1038/sj.mp.4002030
103. Venema, C.M., Mammatas, L.H., van Kruchten, M., Apollonio, G., Schroder, C.P., Glaudemans, A.W., … De Vries, E., (2017). Androgen receptor and estrogen receptor imaging in patients with metastatic breast cancer. Journal of Nuclear Medicine. Advance online publication. doi:10.2967/jnumed.117.193649
104. Videbech, P., Ravnkilde, B., Pedersen, A.R., Egander, A., Landbo, B., Rasmussen, N.A., … Rosenberg, R., (2001). The Danish PET/depression project: PET findings in patients with major depression. Psychological Medicine, 31, 1147–1158. doi:10.1017/S0033291701004469
105. Videbech, P., Ravnkilde, B., Pedersen, T.H., Hartvig, H., Egander, A., Clemmensen, K., … Rosenberg, R., (2002). The Danish PET/depression project: Clinical symptoms and cerebral blood flow. A regions‐of‐interest analysis. Acta Psychiatrica Scandinavica, 106, 35–44. doi:10.1034/j.1600-0447.2002.02245.x
106. Wainwright, S.R., & Galea, L.A., (2013). The neural plasticity theory of depression: assessing the roles of adult neurogenesis and PSA-NCAM within the hippocampus. Neural Plasticity, 2013, 805497. doi:10.1155/2013/805497
107. Wegienka, G., & Baird, D.D., (2005). A comparison of recalled date of last menstrual period with prospectively recorded dates. Journal of Women’s Health, 14, 248–252. doi:10.1089/jwh.2005.14.248
108. Weikum, W.M., Oberlander, T.F., Hensch, T.K., & Werker, J.F., (2012). Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception. Proceedings of the National Academy of Sciences, 109(Suppl 2), 17221–17227.doi:10.1073/pnas.1121263109
109. Weissman, M.M., Bland, R., Joyce, P.R., Newman, S., Wells, J.E., & Wittchen, H.U., (1993). Sex differences in rates of depression: Cross-national perspectives. Journal of Affective Disorders, 29, 77–84.doi:10.1016/0165-0327(93)90025-F
110. Whitton, A.E., Treadway, M.T., & Pizzagalli, D.A., (2015). Reward processing dysfunction in major depression, bipolar disorder and schizophrenia. Current Opinion in Psychiatry, 28, 7. doi:10.1097/YCO.0000000000000122
111. Willner, P., Hale, A.S., & Argyropoulos, S., (2005). Dopaminergic mechanism of antidepressant action in depressed patients. Journal of Affective Disorders, 86, 37–45.doi:10.1016/j.jad.2004.12.010
112. st ed. Geneva: World Health Organization.
113. Xiao, L., & Becker, J.B., (1994). Quantitative microdialysis determination of extracellular striatal dopamine concentration in male and female rats: Effects of estrous cycle and gonadectomy. Neuroscience Letters, 180, 155–158.doi:10.1016/0304-3940(94)90510-X
114. Youdim, M.B., Edmondson, D., & Tipton, K.F., (2006). The therapeutic potential of monoamine oxidase inhibitors. Nature Reviews. Neuroscience, 7, 295. doi:10.1038/nrn1883
115. Young, M.A., Scheftner, W.A., Fawcett, J., & Klerman, G.L., (1990). Gender differences in the clinical features of unipolar major depressive disorder. Journal of Nervous and Mental Disease, 178, 200–203.doi:10.1097/00005053-199003000-00008
116. Young, S.N., Gauthier, S.E.R.G.E., Anderson, G.M., & Purdy, W.C., (1980). Tryptophan, 5-hydroxyindoleacetic acid and indoleacetic acid in human cerebrospinal fluid: Interrelationships and the influence of age, sex, epilepsy and anticonvulsant drugs. Journal of Neurology, Neurosurgery & Psychiatry, 43, 438–445.doi:10.1136/jnnp.43.5.438