Skip to main content
SpringerLink
Log in

Role of estrogen in sex differences in memory, emotion and neuropsychiatric disorders

  • Review
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Estrogen regulates a wide range of neuronal functions in the brain, such as dendritic spine formation, remodeling of synaptic plasticity, cognition, neurotransmission, and neurodevelopment. Estrogen interacts with intracellular estrogen receptors (ERs) and membrane-bound ERs to produce its effect via genomic and non-genomic pathways. Any alterations in these pathways affect the number, size, and shape of dendritic spines in neurons associated with psychiatric diseases. Increasing evidence suggests that estrogen fluctuation causes changes in dendritic spine density, morphology, and synapse numbers of excitatory and inhibitory neurons differently in males and females. In this review, we discuss the role of estrogen hormone in rodents and humans based on sex differences. First, we explain estrogen role in learning and memory and show that a high estrogen level alleviates the deficits in learning and memory. Secondly, we point out that estrogen produces a striking difference in emotional memories in men and women, which leads them to display sex-specific differences in underlying neuronal signaling. Lastly, we discuss that fluctuations in estrogen levels in men and women are related to neuropsychiatric disorders, including schizophrenia, autism spectrum disorder (ASD), attention deficit hyperactivity disorder (ADHD), bipolar disorder (BPD), major depressive disorder (MDD), substance use disorder (SUD), and anxiety disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data and materials availability

All data generated or analyzed during this study are included in the article.

Abbreviations

PFC:

Prefrontal cortex

NAc:

Nucleus accumbens

STR:

Striatum radiatum

mPFC:

Medial prefrontal cortex

EC:

Entorhinal cortex

POA:

Preoptic area

mPOA:

Medial preoptic area (POA)

DLS:

Dorsolateral stratum

ARC:

Arcuate nucleus

VMH:

Ventromedial nucleus

ERα:

Estrogen receptor alpha

ERβ:

Estrogen receptor-beta

GPER:

G-protein coupled estrogen receptor

ERE:

Estrogen responsive element

CA1:

Cornu Ammonis area-1

CA2:

Cornu Ammonis area-2

CA3:

Cornu Ammonis area-3

DG:

Dendate gyrus

ERK:

Extracellular receptor kinase

PKC:

Protein kinase C

PKA:

Protein kinase A

MAPK:

Mitogen activated protein kinase

PI3k:

Akt phosphoinositide 3-kinase

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

NMDA:

N-methyl-d-aspartate

LTP:

Long-term potentiation

LTD:

Long-term depression

OVX:

Ovariectomized

fMRI:

Functional magnetic resonance imaging

BDNF:

Brain-derived neurotrophic factor

TrkB:

Tropomyosin receptor kinase B

PET:

Positron emission tomography

CREB:

CAMP response element binding protein

ERT:

Estrogen replacement therapy

Arc:

Activity-regulated cytoskeleton protein

DHT:

Dihydrotestosterone

SERM:

Selective estrogen receptor modifier

DISC1:

Disrupted-in-schizophrenia 1

CNTNAP2:

Contactin Associated Protein-like 2

iPSC:

Induced pluripotent stem cell

CPP:

Conditioned place preference

HTR7:

Serotonin receptor 7 gene

DA:

Dopamine

CB1R:

Cannabinoid type-1 receptor

mGlu5:

Metabotropic glutamate receptors subtype five

TBI:

Traumatic brain injury

PTSD:

Posttraumatic stress disorder

ASD:

Autism spectrum disorder

BPD:

Bipolar disorder

MDD:

Major depressive disorder

ADHD:

Attention deficit hyperactivity disorder

SUD:

Substance use disorder

GAD:

General anxiety disorder

References

  1. Almey A, Milner TA, Brake WG (2015) Estrogen receptors in the central nervous system and their implication for dopamine-dependent cognition in females. Horm Behav 74:125–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Waters EM et al (2011) Estrogen and aging affect the synaptic distribution of estrogen receptor beta-immunoreactivity in the CA1 region of female rat hippocampus. Brain Res 1379:86–97

    Article  CAS  PubMed  Google Scholar 

  3. Mitra SW et al (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144(5):2055–2067

    Article  CAS  PubMed  Google Scholar 

  4. Mazid S et al (2023) Both nuclear and membrane estrogen receptor alpha impact the expression of estrogen receptors and plasticity markers in the mouse hypothalamus and hippocampus. Biology (Basel) 12(4):632

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Wang YX et al (2019) Postnatal expression patterns of estrogen receptor subtypes and choline acetyltransferase in different regions of the Papez circuit. Dev Neurosci 41(3–4):203–211

    Article  CAS  PubMed  Google Scholar 

  6. Mitrovic N et al (2019) Estrogen receptors modulate ectonucleotidases activity in hippocampal synaptosomes of male rats. Neurosci Lett 712:134474

    Article  CAS  PubMed  Google Scholar 

  7. Fuentes N, Silveyra P (2019) Estrogen receptor signaling mechanisms. Adv Protein Chem Struct Biol 116:135–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Sellers KJ et al (2015) Rapid modulation of synaptogenesis and spinogenesis by 17beta-estradiol in primary cortical neurons. Front Cell Neurosci 9:137

    Article  PubMed  PubMed Central  Google Scholar 

  9. Gegenhuber B et al (2022) Gene regulation by gonadal hormone receptors underlies brain sex differences. Nature 606(7912):153–159

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  10. Finney CA et al (2019) The role of hippocampal estradiol in synaptic plasticity and memory: a systematic review. Front Neuroendocrinol 56:100818

    Article  PubMed  Google Scholar 

  11. Kim J et al (2019) Dorsal hippocampal actin polymerization is necessary for activation of G-protein-coupled estrogen receptor (GPER) to increase CA1 dendritic spine density and enhance memory consolidation. J Neurosci 39(48):9598–9610

    Article  PubMed  PubMed Central  Google Scholar 

  12. Huang Y et al (2023) Brain-derived estrogen regulates neurogenesis, learning and memory with aging in female rats. Biology (Basel) 12(6):760

    CAS  PubMed  Google Scholar 

  13. Potier M et al (2016) Temporal memory and its enhancement by estradiol requires surface dynamics of hippocampal CA1 N-methyl-D-aspartate receptors. Biol Psychiatry 79(9):735–745

    Article  CAS  PubMed  Google Scholar 

  14. Li J et al (2022) Sex differences in memory: do female reproductive factors explain the differences? Front Endocrinol (Lausanne) 13:837852

    Article  PubMed  Google Scholar 

  15. Taxier LR, Gross KS, Frick KM (2020) Oestradiol as a neuromodulator of learning and memory. Nat Rev Neurosci 21(10):535–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Koss WA et al (2018) Sex differences in the rapid cell signaling mechanisms underlying the memory-enhancing effects of 17beta-estradiol. eNeuro 5(5):ENEURO.0267-18.2018

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jacome LF et al (2016) Gonadal hormones rapidly enhance spatial memory and increase hippocampal spine density in male rats. Endocrinology 157(4):1357–1362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sheppard PAS, Puri TA, Galea LAM (2022) Sex differences and estradiol effects in MAPK and Akt cell signaling across subregions of the hippocampus. Neuroendocrinology 112(7):621–635

    Article  CAS  PubMed  Google Scholar 

  19. Lu Y et al (2019) Neuron-derived estrogen regulates synaptic plasticity and memory. J Neurosci 39(15):2792–2809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hokenson RE et al (2021) Unexpected role of physiological estrogen in acute stress-induced memory deficits. J Neurosci 41(4):648–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sheppard PAS et al (2021) Protein synthesis and actin polymerization in the rapid effects of 17beta-estradiol on short-term social memory and dendritic spine dynamics in female mice. Psychoneuroendocrinology 128:105232

    Article  CAS  PubMed  Google Scholar 

  22. Luine V, Serrano P, Frankfurt M (2018) Rapid effects on memory consolidation and spine morphology by estradiol in female and male rodents. Horm Behav 104:111–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hilz EN et al (2019) Mapping the estrous cycle to context-specific extinction memory. Behav Neurosci 133(6):614–623

    Article  CAS  PubMed  Google Scholar 

  24. Tuscher JJ et al (2016) Inhibition of local estrogen synthesis in the hippocampus impairs hippocampal memory consolidation in ovariectomized female mice. Horm Behav 83:60–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wu YW et al (2015) Analyzing the influence of BDNF heterozygosity on spatial memory response to 17beta-estradiol. Transl Psychiatry 5:e498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lan Z et al (2021) Hippocampal aromatase knockdown aggravates ovariectomy-induced spatial memory impairment, Abeta accumulation and neural plasticity deficiency in adult female mice. Neurochem Res 46(5):1188–1202

    Article  CAS  PubMed  Google Scholar 

  27. Spencer JL et al (2008) Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 155(4):1106–1119

    Article  CAS  PubMed  Google Scholar 

  28. Sarvari M et al (2015) Hippocampal gene expression is highly responsive to estradiol replacement in middle-aged female rats. Endocrinology 156(7):2632–2645

    Article  CAS  PubMed  Google Scholar 

  29. Sommer T et al (2018) Effects of the experimental administration of oral estrogen on prefrontal functions in healthy young women. Psychopharmacology 235(12):3465–3477

    Article  CAS  PubMed  Google Scholar 

  30. Patel SA et al (2022) Estradiol effects on spatial memory in women. Behav Brain Res 417:113592

    Article  ADS  CAS  PubMed  Google Scholar 

  31. Hsu CK et al (2021) Gonadal steroid hormones and emotional memory consolidation: a systematic review and meta-analysis. Neurosci Biobehav Rev 130:529–542

    Article  CAS  PubMed  Google Scholar 

  32. Kramar EA et al (2009) Cytoskeletal changes underlie estrogen’s acute effects on synaptic transmission and plasticity. J Neurosci 29(41):12982–12993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Gu J et al (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13(10):1208–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Dominguez R et al (2018) Estradiol protects white matter of male C57BL6J mice against experimental chronic cerebral hypoperfusion. J Stroke Cerebrovasc Dis 27(7):1743–1751

    Article  PubMed  PubMed Central  Google Scholar 

  35. Brann DW et al (2022) Brain-derived estrogen and neural function. Neurosci Biobehav Rev 132:793–817

    Article  CAS  PubMed  Google Scholar 

  36. Russell N et al (2022) Effect of estradiol on cognition in men undergoing androgen deprivation therapy: a randomized placebo-controlled trial. Clin Endocrinol (Oxf) 97(5):622–633

    Article  CAS  PubMed  Google Scholar 

  37. Hernandez-Vivanco A et al (2022) Sex-specific regulation of inhibition and network activity by local aromatase in the mouse hippocampus. Nat Commun 13(1):3913

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  38. Brokling J, Brunne B, Rune GM (2022) Sex-dependent responsiveness of hippocampal neurons to sex neurosteroids: a role of Arc/Arg3.1. J Neuroendocrinol 34(2):e13090

    Article  CAS  PubMed  Google Scholar 

  39. Glover EM, Jovanovic T, Norrholm SD (2015) Estrogen and extinction of fear memories: implications for posttraumatic stress disorder treatment. Biol Psychiatry 78(3):178–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hammoud MZ, Foa EB, Milad MR (2020) Oestradiol, threat conditioning and extinction, post-traumatic stress disorder, and prolonged exposure therapy: a common link. J Neuroendocrinol 32(1):e12800

    Article  CAS  PubMed  Google Scholar 

  41. Gupta RR et al (2001) Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats(1). Brain Res 888(2):356–365

    Article  CAS  PubMed  Google Scholar 

  42. Toufexis DJ et al (2007) Estrogen disrupts the inhibition of fear in female rats, possibly through the antagonistic effects of estrogen receptor alpha (ERalpha) and ERbeta. J Neurosci 27(36):9729–9735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Toufexis DJ, Myers KM, Davis M (2006) The effect of gonadal hormones and gender on anxiety and emotional learning. Horm Behav 50(4):539–549

    Article  CAS  PubMed  Google Scholar 

  44. Guapo VG et al (2009) Effects of sex hormonal levels and phases of the menstrual cycle in the processing of emotional faces. Psychoneuroendocrinology 34(7):1087–1094

    Article  CAS  PubMed  Google Scholar 

  45. Sharma R et al (2021) The regulatory roles of progesterone and estradiol on emotion processing in women. Cogn Affect Behav Neurosci 21(5):1026–1038

    Article  PubMed  Google Scholar 

  46. Staugaard SR, Berntsen D (2021) Gender differences in the experienced emotional intensity of experimentally induced memories of negative scenes. Psychol Res 85(4):1732–1747

    Article  PubMed  Google Scholar 

  47. Kobayashi I et al (2020) Impacts of sex and the estrous cycle on associations between post-fear conditioning sleep and fear memory recall. Behav Brain Res 378:112156

    Article  CAS  PubMed  Google Scholar 

  48. Chen X et al (2005) PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nat Neurosci 8(7):925–931

    Article  CAS  PubMed  Google Scholar 

  49. Herry C et al (2006) Extinction of auditory fear conditioning requires MAPK/ERK activation in the basolateral amygdala. Eur J Neurosci 24(1):261–269

    Article  PubMed  Google Scholar 

  50. Hugues S et al (2006) Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation. Synapse 60(4):280–287

    Article  CAS  PubMed  Google Scholar 

  51. Cover KK et al (2014) Mechanisms of estradiol in fear circuitry: implications for sex differences in psychopathology. Transl Psychiatry 4:e422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Kulkarni J et al (2008) Estrogen in severe mental illness: a potential new treatment approach. Arch Gen Psychiatry 65(8):955–960

    Article  PubMed  Google Scholar 

  53. Sbisa A et al (2020) The effect of 17beta-estradiol on maternal immune activation-induced changes in prepulse inhibition and dopamine receptor and transporter binding in female rats. Schizophr Res 223:249–257

    Article  PubMed  Google Scholar 

  54. Ray P, Mandal N, Sinha VK (2020) Change of symptoms of schizophrenia across phases of menstrual cycle. Arch Womens Ment Health 23(1):113–122

    Article  PubMed  Google Scholar 

  55. Kulkarni J et al (2016) Effect of adjunctive raloxifene therapy on severity of refractory schizophrenia in women: a randomized clinical trial. JAMA Psychiat 73(9):947–954

    Article  Google Scholar 

  56. Seeman MV (2012) Menstrual exacerbation of schizophrenia symptoms. Acta Psychiatr Scand 125(5):363–371

    Article  CAS  PubMed  Google Scholar 

  57. Bergemann N et al (2007) Estrogen, menstrual cycle phases, and psychopathology in women suffering from schizophrenia. Psychol Med 37(10):1427–1436

    Article  PubMed  Google Scholar 

  58. McGregor C, Riordan A, Thornton J (2017) Estrogens and the cognitive symptoms of schizophrenia: possible neuroprotective mechanisms. Front Neuroendocrinol 47:19–33

    Article  CAS  PubMed  Google Scholar 

  59. Wu YC et al (2013) Sex differences and the role of estrogen in animal models of schizophrenia: interaction with BDNF. Neuroscience 239:67–83

    Article  CAS  PubMed  Google Scholar 

  60. McGrath J et al (2004) A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med 2:13

    Article  PubMed  PubMed Central  Google Scholar 

  61. Cotton SM et al (2009) Gender differences in premorbid, entry, treatment, and outcome characteristics in a treated epidemiological sample of 661 patients with first episode psychosis. Schizophr Res 114(1–3):17–24

    Article  CAS  PubMed  Google Scholar 

  62. Hogervorst E et al (2004) Serum levels of estradiol and testosterone and performance in different cognitive domains in healthy elderly men and women. Psychoneuroendocrinology 29(3):405–421

    Article  CAS  PubMed  Google Scholar 

  63. Khodaie-Ardakani MR et al (2015) A placebo-controlled study of raloxifene added to risperidone in men with chronic schizophrenia. Acta Med Iran 53(6):337–345

    PubMed  Google Scholar 

  64. Kulkarni J et al (2013) The role of estrogen in the treatment of men with schizophrenia. Int J Endocrinol Metab 11(3):129–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Ji E et al (2016) Adjunctive selective estrogen receptor modulator increases neural activity in the hippocampus and inferior frontal gyrus during emotional face recognition in schizophrenia. Transl Psychiatry 6:e795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Brand BA et al (2023) The direct and long-term effects of raloxifene as adjunctive treatment for schizophrenia-spectrum disorders: a double-blind randomized clinical trial. Schizophr Bull 49(6):1579–1590

    Article  PubMed  PubMed Central  Google Scholar 

  67. Novick AM et al (2020) Neuropsychiatric effects of tamoxifen: challenges and opportunities. Front Neuroendocrinol 59:100869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Hall J et al (2015) Genetic risk for schizophrenia: convergence on synaptic pathways involved in plasticity. Biol Psychiatry 77(1):52–58

    Article  CAS  PubMed  Google Scholar 

  69. Kirov G et al (2012) De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia. Mol Psychiatry 17(2):142–153

    Article  CAS  PubMed  Google Scholar 

  70. Penzes P et al (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14(3):285–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. MacDonald ML et al (2017) Selective loss of smaller spines in schizophrenia. Am J Psychiatry 174(6):586–594

    Article  PubMed  PubMed Central  Google Scholar 

  72. Arad M, Weiner I (2010) Sex-dependent antipsychotic capacity of 17beta-estradiol in the latent inhibition model: a typical antipsychotic drug in both sexes, atypical antipsychotic drug in males. Neuropsychopharmacology 35(11):2179–2192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Weiser M et al (2019) Effect of adjunctive estradiol on schizophrenia among women of childbearing age: a randomized clinical trial. JAMA Psychiat 76(10):1009–1017

    Article  Google Scholar 

  74. Erli F et al (2020) Estradiol reverses excitatory synapse loss in a cellular model of neuropsychiatric disorders. Transl Psychiatry 10(1):16

    Article  PubMed  PubMed Central  Google Scholar 

  75. Sbisa A, van den Buuse M, Gogos A (2018) The effect of estrogenic compounds on psychosis-like behaviour in female rats. PLoS ONE 13(3):e0193853

    Article  PubMed  PubMed Central  Google Scholar 

  76. Hwang WJ et al (2020) The role of estrogen receptors and their signaling across psychiatric disorders. Int J Mol Sci 22(1)

  77. Weickert TW, Allen KM, Weickert CS (2016) Potential role of oestrogen modulation in the treatment of neurocognitive deficits in schizophrenia. CNS Drugs 30(2):125–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Enriquez KD, Gupta AR, Hoffman EJ (2021) Signaling pathways and sex differential processes in autism spectrum disorder. Front Psychiatry 12:716673

    Article  PubMed  PubMed Central  Google Scholar 

  79. Loomes R, Hull L, Mandy WPL (2017) What is the male-to-female ratio in autism spectrum disorder? A systematic review and meta-analysis. J Am Acad Child Adolesc Psychiatry 56(6):466–474

    Article  PubMed  Google Scholar 

  80. McCarthy MM, Wright CL (2017) Convergence of sex differences and the neuroimmune system in autism spectrum disorder. Biol Psychiatry 81(5):402–410

    Article  CAS  PubMed  Google Scholar 

  81. Chakrabarti B et al (2009) Genes related to sex steroids, neural growth, and social-emotional behavior are associated with autistic traits, empathy, and Asperger syndrome. Autism Res 2(3):157–177

    Article  CAS  PubMed  Google Scholar 

  82. Crider A et al (2014) Dysregulation of estrogen receptor beta (ERbeta), aromatase (CYP19A1), and ER co-activators in the middle frontal gyrus of autism spectrum disorder subjects. Mol Autism 5(1):46

    Article  PubMed  PubMed Central  Google Scholar 

  83. Willsey HR et al (2021) Parallel in vivo analysis of large-effect autism genes implicates cortical neurogenesis and estrogen in risk and resilience. Neuron 109(5):788-804.e8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Xie W et al (2018) Resveratrol ameliorates prenatal progestin exposure-induced autism-like behavior through ERbeta activation. Mol Autism 9:43

    Article  PubMed  PubMed Central  Google Scholar 

  85. Zou Y et al (2017) Prenatal levonorgestrel exposure induces autism-like behavior in offspring through ERbeta suppression in the amygdala. Mol Autism 8:46

    Article  PubMed  PubMed Central  Google Scholar 

  86. Filice F et al (2018) 17-Beta estradiol increases parvalbumin levels in Pvalb heterozygous mice and attenuates behavioral phenotypes with relevance to autism core symptoms. Mol Autism 9:15

    Article  PubMed  PubMed Central  Google Scholar 

  87. Hoffman EJ et al (2016) Estrogens suppress a behavioral phenotype in zebrafish mutants of the autism risk gene, CNTNAP2. Neuron 89(4):725–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Graae L, Karlsson R, Paddock S (2012) Significant association of estrogen receptor binding site variation with bipolar disorder in females. PLoS ONE 7(2):e32304

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  89. Orhan FO et al (2018) Serum levels of GPER-1 in euthymic bipolar patients. Neuropsychiatr Dis Treat 14:855–862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Middle F et al (2003) Variation in the coding sequence and flanking splice junctions of the estrogen receptor alpha (ERalpha) gene does not play an important role in genetic susceptibility to bipolar disorder or bipolar affective puerperal psychosis. Am J Med Genet B Neuropsychiatr Genet 118B(1):72–75

    Article  PubMed  Google Scholar 

  91. Dias RS et al (2011) Longitudinal follow-up of bipolar disorder in women with premenstrual exacerbation: findings from STEP-BD. Am J Psychiatry 168(4):386–394

    Article  PubMed  Google Scholar 

  92. Lyu N et al (2023) Hormonal and inflammatory signatures of different mood episodes in bipolar disorder: a large-scale clinical study. BMC Psychiatry 23(1):449

    Article  PubMed  PubMed Central  Google Scholar 

  93. Perich TA et al (2017) Clinical characteristics of women with reproductive cycle-associated bipolar disorder symptoms. Aust N Z J Psychiatry 51(2):161–167

    Article  PubMed  Google Scholar 

  94. Shi J et al (2008) Neurotransmission and bipolar disorder: a systematic family-based association study. Am J Med Genet B Neuropsychiatr Genet 147B(7):1270–1277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Sigitova E et al (2017) Biological hypotheses and biomarkers of bipolar disorder. Psychiatry Clin Neurosci 71(2):77–103

    Article  PubMed  Google Scholar 

  96. Rosenblat JD, McIntyre RS (2017) Bipolar disorder and immune dysfunction: epidemiological findings, proposed pathophysiology and clinical implications. Brain Sci 7(11):144

    Article  PubMed  PubMed Central  Google Scholar 

  97. Wang LY et al (2018) Systemic autoimmune diseases are associated with an increased risk of bipolar disorder: a nationwide population-based cohort study. J Affect Disord 227:31–37

    Article  PubMed  Google Scholar 

  98. Velez-Perez A et al (2020) Estradiol increases microglial response to lipopolysaccharide in the ventromedial hypothalamus during the peripubertal sensitive period in female mice. eNeuro 7(4):ENEURO.0505-19.2020

    Article  PubMed  PubMed Central  Google Scholar 

  99. Reis de Assis D et al (2021) Using iPSC models to understand the role of estrogen in neuron-glia interactions in schizophrenia and bipolar disorder. Cells 10(2):209

    Article  PubMed  PubMed Central  Google Scholar 

  100. Frey BN, Dias RS (2014) Sex hormones and biomarkers of neuroprotection and neurodegeneration: implications for female reproductive events in bipolar disorder. Bipolar Disord 16(1):48–57

    Article  CAS  PubMed  Google Scholar 

  101. Feng G et al (2019) Neuroendocrine abnormalities associated with untreated first episode patients with major depressive disorder and bipolar disorder. Psychoneuroendocrinology 107:119–123

    Article  CAS  PubMed  Google Scholar 

  102. Wieck A et al (2003) Menstrual cycle effects on hypothalamic dopamine receptor function in women with a history of puerperal bipolar disorder. J Psychopharmacol 17(2):204–209

    Article  CAS  PubMed  Google Scholar 

  103. Matsuoka K et al (2014) Microstructural changes of the nucleus accumbens due to increase of estradiol level during menstrual cycle contribute to recurrent manic episodes—a single case study. Psychiatry Res 221(2):149–154

    Article  PubMed  Google Scholar 

  104. Wei YB et al (2020) A functional variant in the serotonin receptor 7 gene (HTR7), rs7905446, is associated with good response to SSRIs in bipolar and unipolar depression. Mol Psychiatry 25(6):1312–1322

    Article  CAS  PubMed  Google Scholar 

  105. Valvassori SS et al (2017) Lithium and tamoxifen modulate behavior and protein kinase C activity in the animal model of mania induced by ouabain. Int J Neuropsychopharmacol 20(11):877–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Palacios J et al (2019) Tamoxifen for bipolar disorder: systematic review and meta-analysis. J Psychopharmacol 33(2):177–184

    Article  CAS  PubMed  Google Scholar 

  107. Fallah E et al (2016) Effect of tamoxifen and lithium on treatment of acute mania symptoms in children and adolescents. Iran J Child Neurol 10(2):16–25

    MathSciNet  PubMed  PubMed Central  Google Scholar 

  108. Dal-Pont GC et al (2019) Tamoxifen has an anti-manic effect but not protect the brain against oxidative stress in an animal model of mania induced by ouabain. J Psychiatr Res 113:181–189

    Article  PubMed  Google Scholar 

  109. Klann IP, Fulco BCW, Nogueira CW (2023) Subchronic exposure to Tamoxifen modulates the hippocampal BDNF/ERK/Akt/CREB pathway and impairs memory in intact female rats. Chem Biol Interact 382:110615

    Article  CAS  PubMed  Google Scholar 

  110. Young E, Korszun A (2010) Sex, trauma, stress hormones and depression. Mol Psychiatry 15(1):23–28

    Article  CAS  PubMed  Google Scholar 

  111. Gujral S et al (2017) Exercise effects on depression: possible neural mechanisms. Gen Hosp Psychiatry 49:2–10

    Article  PubMed  PubMed Central  Google Scholar 

  112. Burcusa SL, Iacono WG (2007) Risk for recurrence in depression. Clin Psychol Rev 27(8):959–985

    Article  PubMed  PubMed Central  Google Scholar 

  113. Dwyer JB et al (2020) Hormonal treatments for major depressive disorder: state of the art. Am J Psychiatry 177(8):686–705

    Article  PubMed  PubMed Central  Google Scholar 

  114. Duman RS et al (2016) Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants. Nat Med 22(3):238–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Nelson DW et al (2017) Impact of time between diagnosis and SLNB on outcomes in cutaneous melanoma. J Am Coll Surg 225(2):302–311

    Article  PubMed  PubMed Central  Google Scholar 

  116. Endendijk JJ et al (2017) Maternal thyroid hormone trajectories during pregnancy and child behavioral problems. Horm Behav 94:84–92

    Article  CAS  PubMed  Google Scholar 

  117. Kelly SD, Harrell CS, Neigh GN (2014) Chronic stress modulates regional cerebral glucose transporter expression in an age-specific and sexually-dimorphic manner. Physiol Behav 126:39–49

    Article  CAS  PubMed  Google Scholar 

  118. Stevens JS et al (2014) PACAP receptor gene polymorphism impacts fear responses in the amygdala and hippocampus. Proc Natl Acad Sci U S A 111(8):3158–3163

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  119. Chow C et al (2013) Sex differences in neurogenesis and activation of new neurons in response to spatial learning and memory. Psychoneuroendocrinology 38(8):1236–1250

    Article  PubMed  Google Scholar 

  120. Howerton AR et al (2014) Sex differences in corticotropin-releasing factor receptor-1 action within the dorsal raphe nucleus in stress responsivity. Biol Psychiatry 75(11):873–883

    Article  CAS  PubMed  Google Scholar 

  121. Farrell MR, Gruene TM, Shansky RM (2015) The influence of stress and gonadal hormones on neuronal structure and function. Horm Behav 76:118–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. McEwen BS, Gray J, Nasca C (2015) Recognizing resilience: learning from the effects of stress on the brain. Neurobiol Stress 1:1–11

    Article  PubMed  Google Scholar 

  123. Monteggia LM et al (2007) Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors. Biol Psychiatry 61(2):187–197

    Article  CAS  PubMed  Google Scholar 

  124. Dalla C et al (2011) Sex differences in response to stress and expression of depressive-like behaviours in the rat. Curr Top Behav Neurosci 8:97–118

    Article  CAS  PubMed  Google Scholar 

  125. Chhibber A et al (2017) Estrogen receptor beta deficiency impairs BDNF-5-HT2A signaling in the hippocampus of female brain: a possible mechanism for menopausal depression. Psychoneuroendocrinology 82:107–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Perlman WR et al (2005) Alteration in estrogen receptor alpha mRNA levels in frontal cortex and hippocampus of patients with major mental illness. Biol Psychiatry 58(10):812–824

    Article  CAS  PubMed  Google Scholar 

  127. Galea LA, Wide JK, Barr AM (2001) Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav Brain Res 122(1):1–9

    Article  CAS  PubMed  Google Scholar 

  128. Perlman WR et al (2004) Reduced glucocorticoid and estrogen receptor alpha messenger ribonucleic acid levels in the amygdala of patients with major mental illness. Biol Psychiatry 56(11):844–852

    Article  CAS  PubMed  Google Scholar 

  129. Goveas JS et al (2011) Depressive symptoms, brain volumes and subclinical cerebrovascular disease in postmenopausal women: the Women’s Health Initiative MRI Study. J Affect Disord 132(1–2):275–284

    Article  PubMed  PubMed Central  Google Scholar 

  130. Jacobs EG et al (2015) 17beta-Estradiol differentially regulates stress circuitry activity in healthy and depressed women. Neuropsychopharmacology 40(3):566–576

    Article  CAS  PubMed  Google Scholar 

  131. Albert KM et al (2021) Differential effects of estradiol on neural and emotional stress response in postmenopausal women with remitted major depressive disorder. J Affect Disord 293:355–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Findikli E et al (2017) Increased serum G protein-coupled estrogen receptor 1 levels and its diagnostic value in drug naive patients with major depressive disorder. Clin Psychopharmacol Neurosci 15(4):337–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13(10):1161–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Wang Q et al (2017) The recent progress in animal models of depression. Prog Neuropsychopharmacol Biol Psychiatry 77:99–109

    Article  PubMed  PubMed Central  Google Scholar 

  135. Iqbal J et al (2020) Sex difference in depression: which animal models mimic it. Behav Neurosci 134(3):248–266

    Article  CAS  PubMed  Google Scholar 

  136. Shansky RM et al (2004) Estrogen mediates sex differences in stress-induced prefrontal cortex dysfunction. Mol Psychiatry 9(5):531–538

    Article  CAS  PubMed  Google Scholar 

  137. Khayum MA et al (2020) Ovariectomy-induced depressive-like behavior and brain glucose metabolism changes in female rats are not affected by chronic mild stress. Psychoneuroendocrinology 115:104610

    Article  CAS  PubMed  Google Scholar 

  138. Zhang Z et al (2016) Postpartum estrogen withdrawal impairs hippocampal neurogenesis and causes depression- and anxiety-like behaviors in mice. Psychoneuroendocrinology 66:138–149

    Article  CAS  PubMed  Google Scholar 

  139. Slowik A et al (2018) Brain inflammasomes in stroke and depressive disorders: regulation by oestrogen. J Neuroendocrinol 30(2)

  140. Seiffe A et al (2021) Early estradiol exposure masculinizes disease-relevant behaviors in female mice. Eur J Neurosci 53(8):2483–2499

    Article  CAS  PubMed  Google Scholar 

  141. Wu S et al (2020) Long-term supplementation of dehydroepiandrosterone improved depressive-like behaviors by increasing BDNF expression in the hippocampus in ovariectomized rats. Heliyon 6(10):e05180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Ho MF et al (2018) Ketamine and ketamine metabolites as novel estrogen receptor ligands: induction of cytochrome P450 and AMPA glutamate receptor gene expression. Biochem Pharmacol 152:279–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Lipsitz O et al (2021) Intravenous ketamine for postmenopausal women with treatment-resistant depression: results from the Canadian Rapid Treatment Center of Excellence. J Psychiatr Res 136:444–451

    Article  PubMed  Google Scholar 

  144. Rucklidge JJ (2010) Gender differences in attention-deficit/hyperactivity disorder. Psychiatr Clin North Am 33(2):357–373

    Article  PubMed  Google Scholar 

  145. Pinares-Garcia P et al (2018) Sex: a significant risk factor for neurodevelopmental and neurodegenerative disorders. Brain Sci 8(8):154

    Article  PubMed  PubMed Central  Google Scholar 

  146. Quinn PO (2005) Treating adolescent girls and women with ADHD: gender-specific issues. J Clin Psychol 61(5):579–587

    Article  PubMed  Google Scholar 

  147. Lin Y et al (2023) Polymorphism of estrogen receptor genes and its interactions with neurodevelopmental genes in attention deficit hyperactivity disorder among Chinese Han descent. Psychiatry Investig 20(8):775–785

    Article  PubMed  PubMed Central  Google Scholar 

  148. Sahin N et al (2018) Evaluation of estrogen and G protein-coupled estrogen receptor 1 (GPER) levels in drug-naive patients with attention deficit hyperactivity disorder (ADHD). Bosn J Basic Med Sci 18(2):126–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Schug TT et al (2015) Elucidating the links between endocrine disruptors and neurodevelopment. Endocrinology 156(6):1941–1951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Matsuda S et al (2012) Effects of perinatal exposure to low dose of bisphenol A on anxiety like behavior and dopamine metabolites in brain. Prog Neuropsychopharmacol Biol Psychiatry 39(2):273–279

    Article  CAS  PubMed  Google Scholar 

  151. Wilens TE (2008) Effects of methylphenidate on the catecholaminergic system in attention-deficit/hyperactivity disorder. J Clin Psychopharmacol 28(3 Suppl 2):S46-53

    Article  CAS  PubMed  Google Scholar 

  152. Rochester JR, Bolden AL, Kwiatkowski CF (2018) Prenatal exposure to bisphenol A and hyperactivity in children: a systematic review and meta-analysis. Environ Int 114:343–356

    Article  CAS  PubMed  Google Scholar 

  153. Casas M et al (2015) Exposure to bisphenol A during pregnancy and child neuropsychological development in the INMA-Sabadell cohort. Environ Res 142:671–679

    Article  CAS  PubMed  Google Scholar 

  154. Zhou R et al (2011) Abnormal synaptic plasticity in basolateral amygdala may account for hyperactivity and attention-deficit in male rat exposed perinatally to low-dose bisphenol-A. Neuropharmacology 60(5):789–798

    Article  CAS  PubMed  Google Scholar 

  155. Agabio R et al (2016) Sex differences in substance use disorders: focus on side effects. Addict Biol 21(5):1030–1042

    Article  CAS  PubMed  Google Scholar 

  156. Erol A et al (2019) Sex hormones in alcohol consumption: a systematic review of evidence. Addict Biol 24(2):157–169

    Article  CAS  PubMed  Google Scholar 

  157. Hilderbrand ER, Lasek AW (2018) Estradiol enhances ethanol reward in female mice through activation of ERalpha and ERbeta. Horm Behav 98:159–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Vandegrift BJ et al (2020) Estrogen receptor alpha regulates ethanol excitation of ventral tegmental area neurons and binge drinking in female mice. J Neurosci 40(27):5196–5207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Rabiant K et al (2021) Sex difference in the vulnerability to hippocampus plasticity impairment after binge-like ethanol exposure in adolescent rat: is estrogen the key? Addict Biol 26(4):e13002

    Article  CAS  PubMed  Google Scholar 

  160. Martel MM, Eisenlohr-Moul T, Roberts B (2017) Interactive effects of ovarian steroid hormones on alcohol use and binge drinking across the menstrual cycle. J Abnorm Psychol 126(8):1104–1113

    Article  PubMed  PubMed Central  Google Scholar 

  161. Satta R, Hilderbrand ER, Lasek AW (2018) Ovarian hormones contribute to high levels of binge-like drinking by female mice. Alcohol Clin Exp Res 42(2):286–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Vandegrift BJ et al (2017) Estradiol increases the sensitivity of ventral tegmental area dopamine neurons to dopamine and ethanol. PLoS ONE 12(11):e0187698

    Article  PubMed  PubMed Central  Google Scholar 

  163. Khan M, Shah SA, Kim MO (2018) 17beta-Estradiol via SIRT1/Acetyl-p53/NF-kB signaling pathway rescued postnatal rat brain against acute ethanol intoxication. Mol Neurobiol 55(4):3067–3078

    Article  CAS  PubMed  Google Scholar 

  164. Niyomchai T et al (2006) Effects of short- and long-term estrogen and progesterone replacement on behavioral responses and c-fos mRNA levels in female rats after acute cocaine administration. Brain Res 1126(1):193–199

    Article  CAS  PubMed  Google Scholar 

  165. Zhen X et al (2007) Estrogen-modulated frontal cortical CaMKII activity and behavioral supersensitization induced by prolonged cocaine treatment in female rats. Psychopharmacology 191(2):323–331

    Article  CAS  PubMed  Google Scholar 

  166. Febo M, Segarra AC (2004) Cocaine alters GABA(B)-mediated G-protein activation in the ventral tegmental area of female rats: modulation by estrogen. Synapse 54(1):30–36

    Article  CAS  PubMed  Google Scholar 

  167. Park HM et al (2019) Multidimensional top-down proteomics of brain-region-specific mouse brain proteoforms responsive to cocaine and estradiol. J Proteome Res 18(11):3999–4012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Robison CL, Martz JR, Dominguez JM (2018) Influence of preoptic estradiol on behavioral and neural response to cocaine in female Sprague-Dawley rats. Psychopharmacology 235(3):663–672

    Article  CAS  PubMed  Google Scholar 

  169. Febo M et al (2003) Estrogen-dependent alterations in D2/D3-induced G protein activation in cocaine-sensitized female rats. J Neurochem 86(2):405–412

    Article  CAS  PubMed  Google Scholar 

  170. Satta R et al (2018) Estrogen receptor beta in the nucleus accumbens regulates the rewarding properties of cocaine in female mice. Int J Neuropsychopharmacol 21(4):382–392

    Article  CAS  PubMed  Google Scholar 

  171. Doncheck EM et al (2018) 17beta-Estradiol potentiates the reinstatement of cocaine seeking in female rats: role of the prelimbic prefrontal cortex and cannabinoid type-1 receptors. Neuropsychopharmacology 43(4):781–790

    Article  CAS  PubMed  Google Scholar 

  172. Doncheck EM et al (2021) Estradiol regulation of the prelimbic cortex and the reinstatement of cocaine seeking in female rats. J Neurosci 41(24):5303–5314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. d’Adesky ND et al (2018) Nicotine alters estrogen receptor-beta-regulated inflammasome activity and exacerbates ischemic brain damage in female rats. Int J Mol Sci 19(5):1330

    Article  PubMed  PubMed Central  Google Scholar 

  174. Bonansco C et al (2018) Neonatal exposure to oestradiol increases dopaminergic transmission in nucleus accumbens and morphine-induced conditioned place preference in adult female rats. J Neuroendocrinol 30(7):e12574

    Article  CAS  PubMed  Google Scholar 

  175. Sun K et al (2020) Genetic knockout of the G protein-coupled estrogen receptor 1 facilitates the acquisition of morphine-induced conditioned place preference and aversion in mice. Biochem Biophys Res Commun 525(4):1061–1067

    Article  CAS  PubMed  Google Scholar 

  176. McLean CP et al (2011) Gender differences in anxiety disorders: prevalence, course of illness, comorbidity and burden of illness. J Psychiatr Res 45(8):1027–1035

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  177. Kessler RC et al (2017) Trauma and PTSD in the WHO World Mental Health Surveys. Eur J Psychotraumatol 8(suppl 5):1353383

    Article  PubMed  PubMed Central  Google Scholar 

  178. Findikli E et al (2016) Serum levels of G protein-coupled estrogen receptor 1 (GPER1) in drug-naive patients with generalized anxiety disorder. Psychiatry Res 244:312–316

    Article  CAS  PubMed  Google Scholar 

  179. Yen JY et al (2018) Estrogen levels, emotion regulation, and emotional symptoms of women with premenstrual dysphoric disorder: the moderating effect of estrogen receptor 1alpha polymorphism. Prog Neuropsychopharmacol Biol Psychiatry 82:216–223

    Article  CAS  PubMed  Google Scholar 

  180. Liu X et al (2022) Activation of estrogen receptor beta in the lateral habenula improves ovariectomy-induced anxiety-like behavior in rats. Front Behav Neurosci 16:817859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Puga-Olguin A et al (2019) Long-term ovariectomy increases anxiety- and despair-like behaviors associated with lower Fos immunoreactivity in the lateral septal nucleus in rats. Behav Brain Res 360:185–195

    Article  CAS  PubMed  Google Scholar 

  182. Hedges VL et al (2021) Estrogen withdrawal increases postpartum anxiety via oxytocin plasticity in the paraventricular hypothalamus and dorsal raphe nucleus. Biol Psychiatry 89(9):929–938

    Article  CAS  PubMed  Google Scholar 

  183. Hasunuma K et al (2023) Estrogen receptor beta in the lateral septum mediates estrogen regulation of social anxiety-like behavior in male mice. Neuroscience 537:126–140

    Article  PubMed  Google Scholar 

  184. Miller CK et al (2020) Metabotropic glutamate receptor subtype 5 (mGlu5) is necessary for estradiol mitigation of light-induced anxiety behavior in female rats. Physiol Behav 214:112770

    Article  ADS  CAS  PubMed  Google Scholar 

  185. Nillni YI et al (2015) Menstrual cycle effects on psychological symptoms in women with PTSD. J Trauma Stress 28(1):1–7

    Article  PubMed  Google Scholar 

  186. Maddox SA et al (2018) Estrogen-dependent association of HDAC4 with fear in female mice and women with PTSD. Mol Psychiatry 23(3):658–665

    Article  CAS  PubMed  Google Scholar 

  187. Sartin-Tarm A et al (2020) Estradiol modulates neural and behavioral arousal in women with posttraumatic stress disorder during a fear learning and extinction task. Biol Psychiatry Cogn Neurosci Neuroimaging 5(12):1114–1122

    PubMed  PubMed Central  Google Scholar 

  188. Zheng Y et al (2020) GPER-deficient rats exhibit lower serum corticosterone level and increased anxiety-like behavior. Neural Plast 2020:8866187

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  189. Debra A et al (2021) Sex differences in anxiety and depression: circuits and mechanisms. Nature Rev Neurosc 22(11):674–684

  190. Cornish JL et al (2021) Sex differences in substance use disorders: A neurobiological perspective. Front Glob Women’s Health 2:778514. https://doi.org/10.3389/fgwh.2021.778514

  191. Aharonovich E et al (2021) The relationship of frequency of cocaine use to substance and psychiatric disorders in the U.S. general population. Drug Alcohol Depend 227:108933. https://doi.org/10.1016/j.drugalcdep.2021.108933

  192. McGrath JJ et al (2006) Variations in the incidence of schizophrenia: data versus dogma. Schizophrenia Bulletin 32(1):195–197

  193. Gouse BM et al (2022) Improving outcomes in Schizophrenia-A case for initiation of long-acting antipsychotics in early-phase illness. JAMA Network Open 5(7):e2224172

  194. Laws KR et al (2018) Cognitive behavioural therapy for schizophrenia - outcomes for functioning distress and quality of life: a meta-analysis. BMC Psychology 6(1):32. https://doi.org/10.1186/s40359-018-0243-2

  195. Shi B et al (2018) Cognitive, language, and behavioral outcomes in children with autism Spectrum disorders exposed to early comprehensive treatment models: A meta-analysis and meta-regression. Front Psychiatry 12: 691148

  196. Cunningham R et al (2020) Gender and mental health service use in bipolar disorder: national cohort study. BJPsych Open 6(6):e138. https://doi.org/10.1192/bjo.2020.117

  197. Andrade-Gonzalez N et al (2020) The influence of the working alliance on the treatment and outcomes of patients with bipolar disorder: A systematic review. J Affective Disorders 260:263–271. https://doi.org/10.1016/j.jad.2019.09.014

  198. Albert PR (2015) Why is depression more prevalent in women?. J Psychiatry Neurosci 40(4):219-221. https://doi.org/10.1503/jpn.150205

  199. Krause FC et al (2021) Facial emotion recognition in major depressive disorder: A meta-analytic review. J Affective Disorders 293:320–328. https://doi.org/10.1016/j.jad.2021.06.053

  200. Mowlem FD et al (2019) Sex differences in predicting ADHD clinical diagnosis and pharmacological treatment. Eur Child Adolesc Psychiatry 28(4):481–489

  201. Rajaprakash M (2022) Attention-Deficit/Hyperactivity Disorder. Pediatr Rev 43(3):135-147. https://doi.org/10.1542/pir.2020-000612

  202. Slade T (2016) Birth cohort trends in the global epidemiology of alcohol use and alcohol-related harms in men and women: systematic review and metaregression. BMJ Open 6(10):e011827. https://doi.org/10.1136/bmjopen-2016-011827

  203. Katherine MK et al (2008) Evidence for a closing gender gap in alcohol use abuse and dependence in the United States population. Drug Alcohol Depend 93(1-2):21-29. https://doi.org/10.1016/j.drugalcdep.2007.08.017

  204. Aharonovich E (2021) The relationship of frequency of cocaine use to substance and psychiatric disorders in the U.S. general population. Drug and Alcohol Dependence 227:108933. https://doi.org/10.1016/j.drugalcdep.2021.108933

    Article  PubMed  PubMed Central  Google Scholar 

  205. Carmen P., McLean Anu, Asnaani Brett T., Litz Stefan G., Hofmann (2011) Gender differences in anxiety disorders: Prevalence course of illness comorbidity and burden of illness J Psychiatric Res 45(8):1027-1035. https://doi.org/10.1016/j.jpsychires.2011.03.006

Download references

Acknowledgements

Not applicable.

Funding

This work was supported by grants from the National Natural Science Foundation of China (32250410298), the Science and Technology Planning Project of Shenzhen Municipality (KCXFZ20211020164543007, KCXFZ20230731093600002 and 20210617155253001), the Guangdong Basic and Applied Basic Research Foundation (306083115032) and the Shenzhen Fund for Guangdong Provincial High-level Clinical Key Specialties (SZGSP013).

Author information

Authors and Affiliations

  1. Department of Addiction Medicine, Shenzhen Clinical Research Center for Mental Disorders, Shenzhen Kangning Hospital & Shenzhen Mental Health Center, No. 77 Zhenbi Road, Pingshan District, Shenzhen, 518118, Guangdong, China

    Javed Iqbal, Geng-Di Huang, Mei Yang & Xiao-Jian Jia

  2. Clinical College of Mental Health, Shenzhen University Health Science Center, Shenzhen, China

    Mei Yang & Xiao-Jian Jia

  3. Affiliated Mental Health Center, Southern University of Science and Technology, Shenzhen, China

    Mei Yang & Xiao-Jian Jia

  4. National Institute on Drug Dependence and Beijing Key Laboratory of Drug Dependence, Peking University, Beijing, China

    Yan-Xue Xue

Authors
  1. Javed Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geng-Di Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan-Xue Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mei Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiao-Jian Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. JI searched the available literature and prepared the first draft of the manuscript. YXX, MY, GDH, and XJJ commented on previous versions of the manuscript and helped in proofreading. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Mei Yang or Xiao-Jian Jia.

Ethics declarations

Conflict of interest

All authors declare that they have no conflicts of interest concerning the publication of this article.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iqbal, J., Huang, GD., Xue, YX. et al. Role of estrogen in sex differences in memory, emotion and neuropsychiatric disorders. Mol Biol Rep 51, 415 (2024). https://doi.org/10.1007/s11033-024-09374-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11033-024-09374-z

Keywords

Search

Navigation