374
Views
13
CrossRef citations to date
0
Altmetric
Review Article

Sex, stress and the brain: interactive actions of hormones on the developing and adult brain

Pages 18-25 | Received 23 Jul 2014, Accepted 26 Jul 2014, Published online: 16 Sep 2014

References

  • Harris GW. Electrical stimulation of the hypothalamus and the mechanism of neural control of the adenohypophysis. J Physiol 1948;107:418–29
  • Meites J. Short history of neuroendocrinology and the International Society of Neuroendocrinology. Neuroendocrinology 1992;56:1–10
  • Guillemin R. Peptides in the brain: the new endocrinology of the neuron. Science 1978;202:390–402
  • Schally AV, Arimura A, Kastin AJ. Hypothalamic regulatory hormones. Science 1973;179:341–50
  • Jensen E, Geoffrey L, Greene L, Closs LE, Nadji M. Receptors reconsidered: a 20-year perspective. In Greep R, ed. Recent Progress in Hormone Research. New York: Academic Press, 1981:1–40
  • Pfaff DW, Keiner M. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 1973;151:121–58
  • Stumpf WE, Sar M. Steroid hormone target sites in the brain: The differential distribution of estrogen, progestin, androgen and glucocorticosteroid. J Steroid Biochem 1976;7:1163–70
  • Gerlach J, McEwen BS. Rat brain binds adrenal steroid hormone: radioautography of hippocampus with corticosterone. Science 1972;175:1133–6
  • McEwen BS, Plapinger L. Association of corticosterone-1,2 3H with macromolecules extracted from brain cell nuclei. Nature 1970;226:263–4
  • Zigmond R, McEwen BS. Selective retention of oestradiol by cell nuclei in specific brain regions of the ovariectomized rats. J Neurochem 1970;17:889–99
  • Young W. The hormones and mating behavior. In Young W, ed. Sex and Internal Secretions. Baltimore: Williams and Wilkins, 1961:1173–239
  • Davis P, McEwen BS, Pfaff DW. Localized behavioral effects of tritiated estradiol implants in the ventromedial hypothalamus of female rats. Endocrinology 1979;104:898–903
  • Pfaff DW. Estrogens and Brain Function. New York: Springer-Verlag, 1980
  • Bedard PJ, Langelier P, Villeneuve A. Estrogens and the extrapyramidal system. Lancet 1977;2:1367–8
  • McEwen BS, Alves SE, Bulloch K, Weiland NG. Clinically relevant basic science studies of gender differences and sex hormone effects. Psychopharmacol Bull 1998;34:251–9
  • McEwen BS, Alves SH. Estrogen actions in the central nervous system. Endocrine Rev 1999;20:279–307
  • Van Hartesveldt C, Joyce J. Effects of estrogen on the basal ganglia. Neurosci Biobehav Rev 1986;10:1–14
  • Gerlach J, McEwen BS, Pfaff DW, et al. Cells in regions of rhesus monkey brain and pituitary retain radioactive estradiol, corticosterone and cortisol differently. Brain Res 1976;103: 603–12
  • McEwen BS, Weiss J, Schwartz L. Selective retention of corticosterone by limbic structures in rat brain. Nature 1968;220:911–12
  • Eichenbaum H, Otto T. The hippocampus – what does it do? Behav Neural Biol 1992;57:2–36
  • Loy R, Gerlach J, McEwen BS. Autoradiographic localization of estradiol-binding neurons in rat hippocampal formation and entorhinal cortex. Dev Brain Res 1988;39:245–51
  • Kelly MJ, Levin ER. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol Metab 2001;12:152–6
  • McEwen BS, Milner TA. Hippocampal formation: shedding light on the influence of sex and stress on the brain. Brain Res Rev 2007;55:343–55
  • Huhtakangas JA, Olivera CJ, Bishop JE, Zanello LP, Norman AW. The vitamin D receptor is present in caveolae-enriched plasma membranes and binds 1a,25(OH)2-vitamin D3 in vivo and in vitro. Mol Endocrinol 2004;18:2660–71
  • Wehling M, Christ M, Thiesen K. Membrane receptors for aldosterone: a novel pathway for mineralocorticoid action. Am J Physiol 1992;263:E974
  • Tabori NE, Stewart LS, Znamensky V, et al. Ultrastructural evidence that androgen receptors are located at extranuclear sites in the rat hippocampal formation. Neuroscience 2005;130: 151–63
  • Bliss TVP, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973; 232:331–56
  • Parnavelas J, Lynch G, Brecha N, Cotman C, Globus A. Spine loss and regrowth in hippocampus following deafferentation. Nature 1974;248:71–3
  • Bennett E, Diamond M, Krech D, Rosenzweig M. Chemical and anatomical plasticity of brain. Science 1964;146:610–19
  • Greenough WT, Volkmar FR. Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp Neurol 1973;40:491–504
  • Arnold A, Breedlove S. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 1985;19:469–98
  • DeVoogd T, Nottebohm F. Gonadal hormones induce dendritic growth in the adult avian brain. Science 1981;214:202–4
  • Nottebohm F. Why are some neurons replaced in adult brain? J Neurosci 2002;22:624–8
  • Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124:319–36
  • Kaplan MS, Bell DH. Neuronal proliferation in the 9-month-old rodent-radioautographic study of granule cells in the hippocampus. Exp Brain Res 1983;52:1–5
  • Kaplan MS. Environment complexity stimulates visual cortex neurogenesis: death of a dogma and a research career. Trends Neurosci 2001;24:617–20
  • Cameron HA, Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994;61:203–9
  • Gould E, McEwen BS. Neuronal birth and death. Curr Opin Neurobiol 1993;3:676–82
  • Alvarez-Buylla A, Lois C. Neuronal stem cells in the brain of adult vertebrates. Stem Cells 1995;13:263–72
  • Spalding KL, Bergmann O, Alkass K, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell 2013;153: 1219–27
  • Ledoux VA, Smejkalova T, May RM, Cooke BM, Woolley CS. Estradiol facilitates the release of neuropeptide Y to suppress hippocampus-dependent seizures. J Neurosci 2009;29: 1457–68
  • Nakamura NH, McEwen BS. Changes in interneuronal phenotypes regulated by estradiol in the adult rat hippocampus: A potential role for neuropeptide Y. Neuroscience 2005;136: 357–69
  • Terasawa E, Timiras P. Electrical activity during the estrous cycle of the rat: cyclic changes in limbic structures. Endocrinology 1968;83:207–16
  • Sherwin BB. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988;13:345–57
  • Woolley C, Gould E, Frankfurt M, McEwen BS. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 1990;10:4035–9
  • Weiland NG. Estradiol selectively regulates agonist binding sites on the N-methyl-d-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinology 1992;131:662–8
  • Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci 1997; 17:1848–59
  • Huang GZ, Woolley CS. Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism. Neuron 2012;74:801–8
  • Smejkalova T, Woolley CS. Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism. J Neurosci 2010;30:16137–48
  • McEwen BS, Akama KT, Spencer-Segal JL, Milner TA, Waters EM. Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms. Behav Neurosci 2012; 126:4–16
  • Milner TA, Lubbers LS, Alves SE, McEwen BS. Nuclear and extranuclear estrogen binding sites in the rat forebrain and autonomic medullary areas. Endocrinology 2008;149:3306–12
  • Leranth C, Petnehazy O, MacLusky NJ. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J Neurosci 2003;23:1588–92
  • Lewis C, McEwen BS, Frankfurt M. Estrogen-induction of dendritic spines in ventromedial hypothalamus and hippocampus: effects of neonatal aromatase blockade and adult castration. Dev Brain Res 1995;87:91–5
  • MacLusky NJ, Hajszan T, Johansen JA, Jordan CL, Leranth C. Androgen effects on hippocampal CA1 spine synapse numbers are retained in Tfm male rats with defective androgen receptors. Endocrinology 2006;147:2392–8
  • Kerr JE, Allore RJ, Beck SG, Handa RJ. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 1995;136:3213–21
  • Pike CJ, Nguyen T-VV, Ramsden M, Yao M, Murphy MP, Rosario ER. Androgen cell signaling pathways involved in neuroprotective actions. Horm Behav 2008;53:693–705
  • Daniel JM, Dohanich GP. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 2001;21:6949–56
  • Murphy DD, Cole NB, Greenberger V, Segal M. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J Neurosci 1998;18:2550–9
  • Rudick CN, Gibbs RB, Woolley CS. A role for the basal forebrain cholinergic system in estrogen-induced disinhibition of hippocampal pyramidal cells. J Neurosci 2003;23:4479–90
  • Yuen GS, McEwen BS, Akama KT. LIM kinase mediates estrogen action on the actin depolymerization factor Cofilin. Brain Res 2011;1379:44–52
  • Akama KT, McEwen BS. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci 2003;23:2333–9
  • Znamensky V, Akama KT, McEwen BS, Milner TA. Estrogen levels regulate the subcellular distribution of phosphorylated Akt in hippocampal Ca1 dendrites. J Neurosci 2003;23:2340–47
  • Kramar EA, Chen LY, Brandon NJ, et al. Cytoskeletal changes underlie estrogen’s acute effects on synaptic transmission and plasticity. J Neurosci 2009;29:12982–93
  • Christensen A, Dewing P, Micevych P. Membrane-initiated estradiol signaling induces spinogenesis required for female sexual receptivity. J Neurosci 2011;31:17583–9
  • Frankfurt M, Gould E, Wolley C, McEwen BS. Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a golgi study in the adult rat. Neuroendocrinology 1990;51:530–5
  • Frankfurt M, McEwen BS. Estrogen increases axodendritic synapses in the VMN of rats after ovariectomy. NeuroReport 1991;2:380–2
  • Woolley C, McEwen BS. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 1993;336:293–306
  • Parsons B, Rainbow TC, MacLusky N, McEwen BS. Progestin receptor levels in rat hypothalamic and limbic nuclei. J Neurosci 1982;2:1446–52
  • Waters EM, Torres-Revon AT, McEwen BS, Milner TA. Extranuclear progestin receptor immunoreactivity in the rat hippocampal formation. J Comp Neurol 2008;511:34–46
  • Henderson VW, Paganini-Hill A. Oestrogens and Alzheimer’s disease. Ann Prog Reprod Med 1994;2:1–21
  • McCullough LD, Blizzard K, Simpson ER, Oz OK, Hurn PD. Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection. J Neurosci 2003;23:8701–5
  • Nakamura NH, Rosell DR, Akama KT, McEwen BS. Estrogen and ovariectomy regulate mRNA and protein of glutamic acid decarboxylases and cation-chloride cotransporters in the adult rat hippocampus. Neuroendocrinology 2004;80:308–23
  • Nilsen J, Brinton RD. Mitochondria as therapeutic targets of estrogen action in the central nervous system. Curr Drug Targets - CNS & Neurol Disorders 2004;3:297–313
  • Hojo Y, Hattori T-A, Enami T, et al. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc Natl Acad Sci USA 2004;101:865–70
  • Okamoto M, Hojo Y, Inoue K, et al. Mild exercise increases dihydrotestosterone in hippocampus providing evidence for androgenic mediation of neurogenesis. Proc Natl Acad Sci USA 2012;109:13100–5
  • Hao J, Rapp PR, Janssen WGM, et al. Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc Natl Acad Sci USA 2007;104: 11465–70
  • Chen J-R, Yan Y-T, Wang T-J, Chen L-J, Wang Y-J, Tseng G-F. Gonadal hormones modulate the dendritic spine densities of primary cortical pyramidal neurons in adult female rat. Cerebral Cortex 2009;19:2719–27
  • Xiao L, Becker JB. Hormonal activation of the striatum and the nucleus accumbens modulates paced mating behavior in the female rat. Horm Behav 1997;32:114–24
  • Smith SS. Estrogen administration increases neuronal responses to excitatory amino acids as a long-term effect. Brain Res 1989;503:354–57
  • Milner TA, Alves SE, Hayashi S, McEwen BS. An expanded view of estrogen receptor localization in neurons. In Watson CS, ed. The Identities of Membrane Steroid Receptors. Boston, MA: Kluwer Academic Publishers, 2003:21–5
  • Castner SA, Xiao L, Becker JB. Sex differences in striatal dopamine: in vivo microdialysis and behavioral studies. Brain Res 1993;610:127–34
  • Currie LJ, Harrison MB, Trugman JM, Bennett JP, Wooten GF. Postmenopausal estrogen use affects risk for Parkinson disease. Arch Neurol 2004;61:886–8
  • Leranth C, Roth RH, Elswoth JD, Naftolin F, Horvath TL, Redmond DEJ. Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: Implications for Parkinson’s disease and memory. J Neurosci 2000;20:8604–9
  • Bourque M, Dluzen DE, Di Paolo T. Signaling pathways mediating the neuroprotective effects of sex steroids and SERMs in Parkinson’s disease. Front Neuroendocrinol 2012;33: 169–78
  • Bourque M, Morissette M, Cote M, Soulet D, Di Paolo T. Implication of GPER1 in neuroprotection in a mouse model of Parkinson’s disease. Neurobiol Aging 2013;34:887–901
  • Halbreich U, Lumley LA, Palter S, Manning C, Gengo F, Joe S-H. Possible acceleration of age effects on cognition following menopause. J Psychiat Res 1995;29:153–63
  • Sherwin BB. Estrogen and cognitive functioning in women. Endocrine Rev 2003;24:133–51
  • Sherwin BB, Henry JF. Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: a critical review. Front Neuroendocrinol 2008;29: 88–113
  • Hara Y, Yuk F, Puri R, Janssen WG, Rapp PR, Morrison JH. Presynaptic mitochondrial morphology in monkey prefrontal cortex correlates with working memory and is improved with estrogen treatment. Proc Natl Acad Sci USA 2014;111: 486–91
  • Picard M, McEwen BS. Mitochondria impact brain function and cognition. Proc Natl Acad Sci USA 2014;111:7–8
  • Dumitriu D, Hao J, Hara Y, et al. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci 2010; 30:7507–15
  • Dumitriu D, Rapp PR, McEwen BS, Morrison JH. Estrogen and the aging brain: an elixir for the weary cortical network. Ann NY Acad Sci 2010;1204:104–12
  • Bourne JN, Harris KM. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 2008; 31:47–67
  • Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci 2003;26:360–8
  • Galea LAM, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabhar FS. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997;81:689–97
  • Bowman RE, Zrull MC, Luine VN. Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res 2001;904:279–89
  • Luine V, Villegas M, Martinez C, McEwen BS. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 1994;639:167–70
  • Luine VN, Beck KD, Bowman RE, Frankfurt M, MacLusky NJ. Chronic stress and neural function: Accounting for sex and age. J Neuroendocrinol 2007;19:743–51
  • Wood GE, Shors TJ. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc Natl Acad Sci USA 1998;95:4066–71
  • Shors TJ, Miesegaes G. Testosterone in utero and at birth dictates how stressful experience will affect learning in adulthood. Proc Natl Acad Sci USA 2002;99:13955–60
  • Wood GE, Shors TJ, Beylin AV. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behav Neurosci 2001; 115:175–87
  • Leuner B, Mendolia-Loffredo S, Shors TJ. Males and females respond differently to controllability and antidepressant treatment. Biol Psychiat 2004;56:964–70
  • Shansky RM, Hamo C, Hof PR, Lou W, McEwen BS, Morrison JH. Estrogen promotes stress sensitivity in a prefrontal cortex-amygdala pathway. Cereb Cortex 2010;20: 2560–7
  • Bangasser DA, Curtis A, Reyes BA, et al. Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol Psychiatry 2010;15:877–904
  • Bangasser DA, Zhang X, Garachh V, Hanhauser E, Valentino RJ. Sexual dimorphism in locus coeruleus dendritic morphology: A structural basis for sex differences in emotional arousal. Physiol Behav 2011;103:342–51
  • Cahill L. Why sex matters for neuroscience. Nat Rev Neurosci 2006;7:477–84
  • Laje G, Paddock S, Manji H, et al. Genetic markers of suicidal ideation emerging during citalopram treatment of major depression. Am J Psychiatry 2007;164:1530–8
  • McEwen BS. Introduction: The end of sex as we once knew it. Physiol Behav 2009;97:143–5
  • McEwen BS, Lasley EN. The end of sex as we know it. In Cerebrum. The Dana Forum on Brain Science, Vol 7. New York: Dana Press, 2005
  • Carruth LL, Reisert I, Arnold AP. Sex chromosome genes directly affect brain sexual differentiation. Nature Neurosci 2002;5:933–4
  • Derntl B, Finkelmeyer A, Eickhoff S, et al. Multidimensional assessment of empathic abilities: neural correlates and gender differences. Psychoneuroendocrinology 2010;35:67–82
  • McEwen BS. Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 2007;87: 873–904

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.