Advertisement

Neuroimaging Research in Women’s Mental Health: Current Research and Emerging Trends in Women and Transgender Women’s Psychiatry and Mental Health

  • Luciano MinuzziEmail author
  • Maiko A. Schneider
  • Sabrina K. Syan
Chapter
  • 10 Downloads

Abstract

Women’s mental health seems to be affected by different factors and present with particular epidemiology when compared to men’s mental health. In terms of mood disorders, these include the age of onset, seasonal features, incidence of suicidal attempts, and typicality of features. One hypothesis is that the difference in sex hormones is considered to impact the epidemiology and the course of psychiatric disorders in women. For example, changes in the hormonal milieu that occur in the end of pregnancy have been linked to peripartum depression, and the fluctuations of sex hormones during the menstrual cycle have been linked to premenstrual dysphoric disorder (PMDD). Neuroimage research has contributed to identifying potential biomarkers in respect to these disorders. For instance, peripartum depression has been associated with a decreased activation of the limbic structures, as well as a decreased functional connectivity between frontal cortex and limbic structures, which seems to point out different pathophysiologic mechanisms for postpartum depression. Regarding PMDD, being diagnosed with bipolar disorder while experiencing this comorbidity is related to a more challenging course of bipolar disorder. This seems to be related to female sex hormones’ neuroactivity, since they were shown to affect the glutamatergic and GABAergic systems. According to the phase of the menstrual cycle, women with PMDD seem to exhibit different brain activation in the motor and somatosensory cortices. Complementarily, a cortical thickness study showed that PMDD women with bipolar disorder present with an increased cortical thickness of the left superior temporal gyrus, a decreased cortical thickness of the left parietal, and superior frontal and left pericalcarine cortices, including, resting-state functional connectivity (rs-FC) between the left hippocampus and right frontal cortex, as well as decreased rs-FC between right hippocampus and right premotor cortex. Although there are not many neuroimaging studies investigating the influence of “female” sex hormones in the brain, and therefore, their relationship with psychiatric symptoms in transgender women/transgender person should also be considered a population vulnerable to female sex neuroactive steroids influence.

Keywords

Premenstrual dysphoric disorder Peripartum depression Menopause transition Male-to-female transgender Neuroimaging fMRI Bipolar disorder Depression 

References

  1. 1.
    Levin JM, Frederick BD, Ross MH, Fox JF, von Rosenberg HL, Kaufman MJ, et al. Influence of baseline hematocrit and hemodilution on BOLD fMRI activation. Magn Reson Imaging. 2001;19(8):1055–62.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Weissenbacher A, Kasess C, Gerstl F, Lanzenberger R, Moser E, Windischberger C. Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. NeuroImage. Elsevier Inc; 2009;47(4):1408–16.Google Scholar
  3. 3.
    Hart MG, Price SJ, Suckling J. Connectome analysis for pre-operative brain mapping in neurosurgery. Br J Neurosurg. 1st ed. 2016;30(5):506–17.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Sacher J, Neumann J, Fünfstück T, Soliman A, Villringer A, Schroeter ML. Mapping the depressed brain: a meta-analysis of structural and functional alterations in major depressive disorder. J Affect Disord. Elsevier B.V; 2012;140(2):142–8.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Barrett J, Wonch KE, Gonzalez A, Ali N, Steiner M, Hall GB, et al. Maternal affect and quality of parenting experiences are related to amygdala response to infant faces. Soc Neurosci. 3rd ed. 2012;7(3):252–68.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Gingnell M, Toffoletto S, Wikström J, Engman J, Bannbers E, Comasco E, et al. Emotional anticipation after delivery – a longitudinal neuroimaging study of the postpartum period. Sci Rep. Springer US; 2017;7(1):114.Google Scholar
  7. 7.
    Silverman ME, Loudon H, Safier M, Protopopescu X, Leiter G, Liu X, et al. Neural dysfunction in postpartum depression: an fMRI pilot study. CNS Spectr. University of Arizona; 2007;12(11):853–62.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Silverman ME, Loudon H, Liu X, Mauro C, Leiter G, Goldstein MA. The neural processing of negative emotion postpartum: a preliminary study of amygdala function in postpartum depression. Arch Womens Ment Health. 2011;14(4):355–9.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Chase HW, Moses-Kolko EL, Zevallos C, Wisner KL, Phillips ML. Disrupted posterior cingulate–amygdala connectivity in postpartum depressed women as measured with resting BOLD fMRI. Soc Cogn Affect Neurosci. 2014;9(8):1069–75.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Wonch KE, de Medeiros CB, Barrett JA, Dudin A, Cunningham WA, Hall GB, et al. Postpartum depression and brain response to infants: differential amygdala response and connectivity. Soc Neurosci. Routledge; 2016;11(6):600–17.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Deligiannidis KM, Sikoglu EM, Shaffer SA, Frederick B, Svenson AE, Kopoyan A, et al. GABAergic neuroactive steroids and resting-state functional connectivity in postpartum depression: a preliminary study. J Psychiatr Res. Elsevier Ltd; 2013;47(6):816–28.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    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. 2010;167(11):1373–80.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Moses-Kolko EL, Fraser D, Wisner KL, James JA, Saul AT, Fiez JA, et al. Rapid habituation of ventral striatal response to reward receipt in postpartum depression. Biol Psychiatry. Elsevier Inc; 2011;70(4):395–9.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Xiao-juan W, Jian W, Zhi-hong L, Yan M, Shi-wei Z. Increased posterior cingulate, medial frontal and decreased temporal regional homogeneity in depressed mothers. A resting-state functional magnetic resonance study. Procedia Environ Sci. 2011;8:737–43.CrossRefGoogle Scholar
  15. 15.
    Laurent HK, Ablow JC. A cry in the dark: depressed mothers show reduced neural activation to their own infant’s cry. Soc Cogn Affect Neurosci. 2011;7(2):125–34.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Helm K, Viol K, Weiger TM, Tass PA, Grefkes C, del Monte D, et al. Neuronal connectivity in major depressive disorder: a systematic review. Neuropsychiatr Dis Treat. 2018;14:2715–37.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Farage MA, Neill S, MacLean AB. Physiological changes associated with the menstrual cycle. Obstet Gynecol Surv. 2009;64(1):58–72.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Soares CN, Zitek B. Reproductive hormone sensitivity and risk for depression across the female life cycle: a continuum of vulnerability? J Psychiatry Neurosci. 2008;33(4):331–43.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Weiser MJ, Foradori CD, Handa RJ. Estrogen receptor beta in the brain: from form to function. Brain Res Rev. 2008;57(2):309–20.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Österlund M, Kuiper GGJM, Gustafsson J-Å, Hurd YL. Differential distribution and regulation of estrogen receptor-α and -β mRNA within the female rat brain. Mol Brain Res. 1998;54(1):175–80.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Osterlund MK, Gustafsson JA, Keller E, Hurd YL. Estrogen receptor beta (ERbeta) messenger ribonucleic acid (mRNA) expression within the human forebrain: distinct distribution pattern to ERalpha mRNA. J Clin Endocrinol Metabol. 2000;85(10):3840–6.Google Scholar
  22. 22.
    Bixo M, Bäckström T, Winblad B, Andersson A. Estradiol and testosterone in specific regions of the human female brain in different endocrine states. J Steroid Biochem Mol Biol. 1995;55(3–4):297–303.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Lokuge S, Frey BN, Foster JA, Soares CN, Steiner M. The rapid effects of estrogen: a mini-review. Behav Pharmacol. 2010;21(5–6):465–72.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Bixo M, Andersson A, Winblad B, Purdy RH, Bäckström T. Progesterone, 5-pregnane-3,20-dione and 3-hydroxy-5-pregnane-20-one in specific regions of the human female brain in different endocrine states. Brain Res. 1997;764(1–2):173–8.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Giatti S, Melcangi RC, Pesaresi M. The other side of progestins: effects in the brain. J Mol Endocrinol. 2016;57(2):R109–26.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Bitran D, Shiekh M, McLeod M. Anxiolytic effect of progesterone is mediated by the neurosteroid allopregnanolone at brain GABAA receptors. J Neuroendocrinol. 1995;7(3):171–7.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Bäckström T, Bixo M, Johansson M, Nyberg S, Ossewaarde L, Ragagnin G, et al. Allopregnanolone and mood disorders. Prog Neurobiol. Elsevier Ltd; 2014;113:88–94.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Sundström Poromaa I, Smith S, Gulinello M. GABA receptors, progesterone and premenstrual dysphoric disorder. Arch Womens Ment Health. 2003;6(1):23–41.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Vigod SN, Frey BN, Soares CN, Steiner M. Approach to premenstrual dysphoria for the mental health practitioner. Psychiatr Clin North Am. 2010;33(2):257–72.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Nyberg S, Wahlström G, Bäckström T, Poromaa IS. Altered sensitivity to alcohol in the late luteal phase among patients with premenstrual dysphoric disorder. Psychoneuroendocrinology. 2004;29(6):767–77.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Gartside SE, Griffith NC, Kaura V, Ingram CD. The neurosteroid dehydroepiandrosterone (DHEA) and its metabolites alter 5-HT neuronal activity via modulation of GABA Areceptors. J Psychopharmacol. 2010;24(11):1717–24.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    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.CrossRefGoogle Scholar
  34. 34.
    Halbreich U, Borenstein J, Pearlstein T, Kahn LS. The prevalence, impairment, impact, and burden of premenstrual dysphoric disorder (PMS/PMDD). Psychoneuroendocrinology. 2003;28:1–23.Google Scholar
  35. 35.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Treloar SA, Heath AC, Martin NG. Genetic and environmental influences on premenstrual symptoms in an Australian twin sample. Psychol Med. 2002;32(1):25–38.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Pearlstein T, Steiner M. Premenstrual dysphoric disorder: burden of illness and treatment update. J Psychiatry Neurosci. 2008;33(4):291–301.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Beck LE, Gevirtz R, Mortola JF. The predictive role of psychosocial stress on symptom severity in premenstrual syndrome. Psychosom Med. 1990;52(5):536–43.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Bäckström T, Haage D, Löfgren M, Johansson IM, Strömberg J, Nyberg S, et al. Review paradoxical effects of GABA-A modulators may explain sex steroid induced negative mood symptoms in some persons. Neuroscience. Elsevier Inc; 2011;191(C):46–54.Google Scholar
  40. 40.
    Jacobs E, D’Esposito M. Estrogen shapes dopamine-dependent cognitive processes: implications for women’s health. J Neurosci. 2011;31(14):5286–93.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ismaili E, Walsh S, O’Brien PMS, Bäckström T, Brown C, Dennerstein L, et al. Fourth consensus of the International Society for Premenstrual Disorders (ISPMD): auditable standards for diagnosis and management of premenstrual disorder. Arch Womens Ment Health. 2016;19(6):953–8.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Rapkin AJ, Edelmuth E, Chang LC, Reading AE, McGuire MT, Su TP. Whole-blood serotonin in premenstrual syndrome. Obstet Gynecol. 1987;70(4):533–7.PubMedPubMedCentralGoogle Scholar
  43. 43.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Jeong H-G, Ham B-J, Bin Yeo H, Jung I-K, Joe S-H. Gray matter abnormalities in patients with premenstrual dysphoric disorder: an optimized voxel-based morphometry. J Affect Disord. Elsevier B.V; 2012;140(3):260–7.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Rapkin AJ, Berman SM, Mandelkern MA, Silverman DHS, Morgan M, London ED. Neuroimaging evidence of cerebellar involvement in premenstrual dysphoric disorder. Biol Psychiatry. 2011;69(4):374–80.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Rapkin AJ, Berman SM, London ED, USA David Geffen School of Medicine at UCLA, Box 951740, 27-139 CHS, Los Angeles, CA90095, USA Email: ARapkin@mednet.ucla.edu. The cerebellum and premenstrual dysphoric disorder. AIMS Neurosci. 2014;1(2):120–41.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Petersen N, Ghahremani DG, Rapkin AJ, Berman SM, Liang L, London ED. Brain activation during emotion regulation in women with premenstrual dysphoric disorder. Psychol Med. 2018;48(11):1795–802.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Protopopescu X, Tuescher O, Pan H, Epstein J, Root J, Chang L, et al. Toward a functional neuroanatomy of premenstrual dysphoric disorder. J Affect Disord. 2008;108(1–2):87–94.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Jogia J, Dima D, Frangou S. Sex differences in bipolar disorder: a review of neuroimaging findings and new evidence. Bipolar Disord. 2012;14(4):461–71.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Rasgon N, Bauer M, Grof P, Gyulai L, Elman S, Glenn T, et al. Sex-specific self-reported mood changes by patients with bipolar disorder. J Psychiatr Res. 2005;39(1):77–83.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Kawa I, Carter JD, Joyce PR, Doughty CJ, Frampton CM, Wells JE, et al. Gender differences in bipolar disorder: age of onset, course, comorbidity, and symptom presentation. Bipolar Disord. 2005;7(2):119–25.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Diflorio A, Jones I. Is sex important? Gender differences in bipolar disorder. Int Rev Psychiatry. 2010;22(5):437–52.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Miller LJ, Ghadiali NY, Larusso EM, Wahlen KJ, Avni-Barron O, Mittal L, et al. Bipolar disorder in women. Health Care Women Int. 2014;36(4):475–98.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Frye MA, Altshuler LL, McElroy SL, Suppes T, Keck PE, Denicoff K, et al. Gender differences in prevalence, risk, and clinical correlates of alcoholism comorbidity in bipolar disorder. Am J Psychiatry. 2003;160(5):883–9.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Choi J, Baek JH, Noh J, Kim JS, Choi JS, Ha K, et al. Association of seasonality and premenstrual symptoms in Bipolar I and Bipolar II disorders. J Affect Disord. Elsevier B.V; 2011;129(1–3):313–6.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Fornaro M, Perugi G. The impact of premenstrual dysphoric disorder among 92 bipolar patients. Eur Psychiatry. Elsevier Masson SAS; 2010;25(8):450–4.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Dias RS, Lafer B, Russo C, Del Debbio A, Nierenberg AA, Sachs GS, et al. Longitudinal follow-up of bipolar disorder in women with premenstrual exacerbation: findings from STEP-BD. Am J Psychiatry. 2011;168(4):386–94.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Frey BN, Dias RS. Sex hormones and biomarkers of neuroprotection and neurodegeneration: implications for female reproductive events in bipolar disorder. Bipolar Disord. 2013;16(1):48–57.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Robakis TK, Holtzman J, Stemmle PG, Reynolds-May MF, Kenna HA, Rasgon NL. Lamotrigine and GABAA receptor modulators interact with menstrual cycle phase and oral contraceptives to regulate mood in women with bipolar disorder. J Affect Disord. 2015;175:108–15.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Toffoletto S, Lanzenberger R, Gingnell M, Sundström-Poromaa I, Comasco E. Emotional and cognitive functional imaging of estrogen and progesterone effects in the female human brain: a systematic review. Psychoneuroendocrinology. Elsevier Ltd; 2014;50:28–52.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Strakowski SM, Adler CM, Almeida J, Altshuler LL, Blumberg HP, Chang KD, et al. The functional neuroanatomy of bipolar disorder: a consensus model. Bipolar Disord. 2012;14(4):313–25.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Reynolds-May MF, Kenna HA, Marsh W, Stemmle PG, Wang P, Ketter TA, et al. Evaluation of reproductive function in women treated for bipolar disorder compared to healthy controls. Bipolar Disord. 2013;16(1):37–47.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Lee H, Park J, Choi B, Yi H, Kim S-S. Experiences of and barriers to transition-related healthcare among Korean transgender adults: focus on gender identity disorder diagnosis, hormone therapy, and sex reassignment surgery. Epidemiol Health. 2018;40:e2018005–13.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Slyepchenko A, Frey BN, Lafer B, Nierenberg AA, Sachs GS, Dias RS. Increased illness burden in women with comorbid bipolar and premenstrual dysphoric disorder: data from 1 099 women from STEP-BD study. Acta Psychiatr Scand. John Wiley & Sons, Ltd (10.1111); 2017;136(5):473–82.Google Scholar
  65. 65.
    Connolly MD, Zervos MJ, Barone II CJ, Johnson CC, Joseph CL. The mental health of transgender youth: advances in understanding. J Adolesc Health. Elsevier Inc; 2016;59(5):489–95.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Heylens G, Elaut E, Kreukels BPC, Paap MCS, Cerwenka S, Richter-Appelt H, et al. Psychiatric characteristics in transsexual individuals: multicentre study in four European countries. Br J Psychiatry. 2018;204(02):151–6.CrossRefGoogle Scholar
  67. 67.
    Swaab DF. Sexual differentiation of the brain and behavior. Best Pract Res Clin Endocrinol Metab. 2007;21(3):431–44.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Mueller SC, Landré L, Wierckx K, T’Sjoen G. A structural magnetic resonance imaging study in transgender persons on cross-sex hormone therapy. Neuroendocrinology. 2017;105(2):123–30.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Savic I, Arver S. Sex differences in cortical thickness and their possible genetic and sex hormonal underpinnings. Cereb Cortex. 2013;24(12):3246–57.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Syan SK, Minuzzi L, Smith M, Costescu D, Allega OR, Hall GBC, et al. Brain structure and function in women with comorbid bipolar and premenstrual dysphoric disorder. Front Psych. 2018;8:241–13.Google Scholar
  71. 71.
    Reed GM, Drescher J, Krueger RB, Atalla E, Cochran SD, First MB, et al. Disorders related to sexuality and gender identity in the ICD-11: revising the ICD-10 classification based on current scientific evidence, best clinical practices, and human rights considerations. World Psychiatry. 5 ed. Wiley-Blackwell; 2016;15(3):205–21.Google Scholar
  72. 72.
    Soll BM, Robles-García R, Brandelli-Costa A, Mori D, Mueller A, Vaitses-Fontanari AM, et al. Gender incongruence: a comparative study using ICD-10 and DSM-5 diagnostic criteria. Rev Bras Psiquiatr. 8 ed. 2017;24(0):568–7.Google Scholar
  73. 73.
    Beek TF, Cohen-Kettenis PT, Kreukels BPC. Gender incongruence/gender dysphoria and its classification history. Int Rev Psychiatry. 3rd ed. 2016;28(1):5–12.Google Scholar
  74. 74.
    Hembree WC, Cohen-Kettenis PT, Gooren L, Hannema SE, Meyer WJ, Murad MH, et al. Endocrine treatment of gender-dysphoric/gender-incongruent persons: an endocrine society clinical practice guideline. 6 ed. J Clin Endocrinol Metabol. 2017;102:3869–903.CrossRefGoogle Scholar
  75. 75.
    da Silva DC, Schwarz K, Fontanari AM, Costa AB, Massuda R, Henriques AA, Salvador J, Silveira E, Rosito TE, Lobato MI WHOQOL-100 before and after sex reassignment surgery in Brazilian male-to-female transsexual individuals. J Sex Med. Elsevier Inc; 2016;13(6):988–93.Google Scholar
  76. 76.
    Gorin-Lazard A, Baumstarck K, Boyer L, Maquigneau A, Penochet J-C, Pringuey D, et al. Hormonal therapy is associated with better self-esteem, mood, and quality of life in transsexuals. J Nerv Ment Dis. 2013;201(11):996–1000.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Bartolucci C, Gómez-Gil E, Salamero M, Esteva I, Guillamon A, Zubiaurre L, et al. Sexual quality of life in gender-dysphoric adults before genital sex reassignment surgery. J Sex Med. 2015;12(1):180–8.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Tucker RP, Testa RJ, Simpson TL, Shipherd JC, Blosnich JR, Lehavot K. Hormone therapy, gender affirmation surgery, and their association with recent suicidal ideation and depression symptoms in transgender veterans. Psychol Med. 2018;48(14):2329–36.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Nota NM, Burke SM, den Heijer M, Soleman RS, Lambalk CB, Cohen-Kettenis PT, et al. Brain sexual differentiation and effects of cross-sex hormone therapy in transpeople: a resting-state functional magnetic resonance study. Clin Neurophysiol. Elsevier Masson SAS; 2017;47(5–6):361–70.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Luders E, Sánchez FJ, Tosun D, Shattuck DW, Gaser C, Vilain E, et al. Increased cortical thickness in male-to-female transsexualism. J Behav Brain Sci. 2012;02(03):357–62.CrossRefGoogle Scholar
  81. 81.
    Rametti G, Carrillo B, Gómez-Gil E, Junque C, Zubiaurre-Elorza L, Segovia S, et al. Effects of androgenization on the white matter microstructure of female-to-male transsexuals. A diffusion tensor imaging study. Psychoneuroendocrinology. 2012;37(8):1261–9.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Zubiaurre-Elorza L, Junque C, Gomez-Gil E, Segovia S, Carrillo B, Rametti G, et al. Cortical thickness in untreated transsexuals. Cereb Cortex. 2013;23(12):2855–62.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Luders E, Sánchez FJ, Gaser C, Toga AW, Narr KL, Hamilton LS, et al. Regional gray matter variation in male-to-female transsexualism. NeuroImage. Elsevier Inc; 2009;46(4):904–7.Google Scholar
  84. 84.
    Pol HEH, Cohen-Kettenis PT, Van Haren NEM, Peper JS, Brans RGH, Cahn W, et al. Changing your sex changes your brain: influences of testosterone and estrogen on adult human brain structure. Eur J Endocrinol. 2006;155(suppl_1):S107–14.CrossRefGoogle Scholar
  85. 85.
    Nguyen HB, Loughead J, Lipner E, Hantsoo L, Kornfield SL, Epperson CN. What has sex got to do with it? The role of hormones in the transgender brain. Neuropsychopharmacology. Springer US; 2019;44(1):22..CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Kreukels BPC, Guillamon A. Neuroimaging studies in people with gender incongruence. Int Rev Psychiatry. 10 ed. 2016;28(1):120–8.CrossRefPubMedGoogle Scholar
  87. 87.
    Mueller SC, Wierckx K, Jackson K, T’Sjoen G. Circulating androgens correlate with resting-state MRI in transgender men. Psychoneuroendocrinology. Elsevier Ltd; 2016;73:91–8.Google Scholar
  88. 88.
    Spizzirri G, Duran FXBLS, Chaim-Avancini TM, Serpa MH, Cavallet M, Pereira CMA, et al. Grey and white matter volumes either in treatment-naïve or hormone-treated transgender women: a voxel-based morphometry study. Sci Rep. Springer US; 2018;8(1):736.Google Scholar
  89. 89.
    Burke SM, Manzouri AH, Dhejne C, Bergström K, Arver S, Feusner JD, et al. Testosterone effects on the brain in transgender men. Cereb Cortex. 6 ed. 2017;13(6):1–15.Google Scholar
  90. 90.
    Seiger R, Hahn A, Hummer A, Kranz GS, Ganger S, Woletz M, et al. Subcortical gray matter changes in transgender subjects after long-term cross-sex hormone administration. Psychoneuroendocrinology. Elsevier Ltd; 2016;74:371–9.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Ritchie SJ, Cox SR, Shen X, Lombardo MV, Reus LM, Alloza C, et al. Sex differences in the adult human brain: evidence from 5216 UK Biobank participants. Cereb Cortex. 2018;60(4):565–17.Google Scholar
  92. 92.
    Zubiaurre-Elorza L, Junque C, Gómez-Gil E, Guillamon A. Effects of cross-sex hormone treatment on cortical thickness in transsexual individuals. J Sex Med. 2014;11(5):1248–61.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Kuperberg GR, Broome MR, McGuire PK, David AS, Eddy M, Ozawa F, et al. Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry. American Medical Association; 2003;60(9):878–88.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Savic I, Frisen L, Manzouri A, Nordenstrom A, Lindén Hirschberg A. Role of testosterone and Y chromosome genes for the masculinization of the human brain. Hum Brain Mapp. 2017;38(4):1801–14.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Savic I, Arver S. Sex differences in cortical thickness and their possible genetic and sex hormonal underpinnings. Cereb Cortex. Oxford University Press; 2014;24(12):3246–57.Google Scholar
  96. 96.
    Wickens MM, Bangasser DA, Briand LA. Sex differences in psychiatric disease: a focus on the glutamate system. Front Mol Neurosci. 2018;11:417–2.CrossRefGoogle Scholar
  97. 97.
    Swift-Gallant A, Monks DA. Androgenic mechanisms of sexual differentiation of the nervous system and behavior. Front Neuroendocrinol. 2017;46:32–45.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Bos PA, Panksepp J, Bluthé R-M, van Honk J. Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: a review of single administration studies. Front Neuroendocrinol. Elsevier Inc; 2012;33(1):17–35.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Feusner JD, Lidström A, Moody TD, Dhejne C, Bookheimer SY, Savic I. Intrinsic network connectivity and own body perception in gender dysphoria. Brain Imaging Behav. 2017;11(4):964–76.CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Lin C-S, Ku H-L, Chao H-T, Tu P-C, Li C-T, Cheng C-M, et al. Neural network of body representation differs between transsexuals and cissexuals. Urgesi C, editor. PLoS One. 2014;9(1):e85914–0.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Schneider MA, Andreazza T, Fontanari AMV, Costa AB, Silva DCD, de Aguiar BW, et al. Serum concentrations of brain-derived neurotrophic factor in patients diagnosed with gender dysphoria undergoing sex reassignment surgery. Trends Psychiatry Psychother. 2017;39(1):43–7.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Fuss J, Hellweg R, Van Caenegem E, Briken P, Stalla GK, T’Sjoen G, et al. Cross-sex hormone treatment in male-to-female transsexual persons reduces serum brain-derived neurotrophic factor (BDNF). Eur Neuropsychopharmacol. Elsevier; 2015;25(1):95–9.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Fontanari AMV, Costa AB, Aguiar B, Tusset C, Andreazza T, Schneider M, et al. Reduced serum concentrations of brain-derived neurotrophic factor (BDNF) in transsexual Brazilian men. Neurosci Lett. 2016;630:109–13.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Luciano Minuzzi
    • 1
    Email author
  • Maiko A. Schneider
    • 1
  • Sabrina K. Syan
    • 2
  1. 1.Department of Psychiatry and Behavioural NeurosciencesMcMaster UniversityHamiltonCanada
  2. 2.Department of Psychiatry and Behavioural Neurosciences & Department of Psychology, Neuroscience and BehaviourMcMaster UniversityHamiltonCanada

Personalised recommendations