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Dose-dependent effects of estrogen on prediction error related neural activity in the nucleus accumbens of healthy young women

  • Janine BayerEmail author
  • Tessa Rusch
  • Lei Zhang
  • Jan Gläscher
  • Tobias Sommer
Original Investigation

Abstract

Rationale

Whereas the effect of the sex steroid 17-beta-estradiol (E2) on dopaminergic (DA) transmission in the nucleus accumbens (NAc) is well evidenced in female rats, studies in humans are inconsistent. Moreover, linear and inverted u-shaped dose response curves have been observed for E2’s effects on hippocampal plasticity, but the shape of dose response curves for E2’s effects on the NAc is much less characterized.

Objectives

Investigation of dose response curves for E2’s effects on DA-related neural activity in the human NAc.

Methods

Placebo or E2 valerate in doses of 2, 4, 6 or 12 mg was orally administered to 125 naturally cycling young women during the low-hormone menstruation phase on two consecutive days using a randomized, double-blinded design. The E2 treatment regimen induced a wide range of E2 levels, from physiological (2- and 4-mg groups; equivalent to cycle peak) to supraphysiological levels (6- and 12-mg groups; equivalent to early pregnancy). This made it possible to study different dose response functions for E2’s effects on NAc activity. During E2 peak, participants performed a well-established reversal learning paradigm. We used trial-wise prediction errors (PE) estimated via a computational reinforcement learning model as a proxy for dopaminergic activity. Linear and quadratic regression analyses predicting PE-related NAc activity from salivary E2 levels were calculated.

Results

There was a positive linear relationship between PE-associated NAc activity and salivary E2 increases.

Conclusions

The randomized, placebo-controlled elevation of E2 levels stimulates NAc activity in the human brain, likely mediated by dopaminergic processes.

Keywords

Estrogen Reward Prediction error fMRI Ventral striatum 

Notes

Funding information

This work was supported by the German Research Foundation (DFG SO 952/6-1). J.G. was funded by SFB TRR 169 ‘Crossmodal Learning’ and the Bernstein Award for Computational Neuroscience (BMBF grant 01GQ1003).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

213_2019_5409_MOESM1_ESM.doc (1.1 mb)
ESM 1 (DOC 1154 kb)

References

  1. Abler B, Walter H, Erk S, Kammerer H, Spitzer M (2006) Prediction error as a linear function of reward probability is coded in human nucleus accumbens. NeuroImage 31:790–795.  https://doi.org/10.1016/j.neuroimage.2006.01.001 CrossRefPubMedGoogle Scholar
  2. Almey A, Filardo EJ, Milner TA, Brake WG (2012) Estrogen receptors are found in glia and at extranuclear neuronal sites in the dorsal striatum of female rats: evidence for cholinergic but not dopaminergic colocalization. Endocrinology 153:5373–5383.  https://doi.org/10.1210/en.2012-1458 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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.  https://doi.org/10.1016/j.yhbeh.2015.06.010 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alonso-Alonso M, Ziemke F, Magkos F, Barrios FA, Brinkoetter M, Boyd I, Rifkin-Graboi A, Yannakoulia M, Rojas R, Pascual-Leone A, Mantzoros CS (2011) Brain responses to food images during the early and late follicular phase of the menstrual cycle in healthy young women: relation to fasting and feeding. Am J Clin Nutr 94:377–384.  https://doi.org/10.3945/ajcn.110.010736 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bakkum BW, Fan L, Pandey SC, Cohen RS (2011) Hetereogeneity of dose and time effects of estrogen on neuron-specific neuronal protein and phosphorylated cyclic AMP response element-binding protein in the hippocampus of ovariectomized rats. J Neurosci Res 89:883–897.  https://doi.org/10.1002/jnr.22601 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Barth C, Villringer A, Sacher J (2015) Sex hormones affect neurotransmitters and shape the adult female brain during hormonal transition periods. Front Neurosci 9.  https://doi.org/10.3389/fnins.2015.00037
  7. Bayer HM, Glimcher PW (2005) Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47:129–141.  https://doi.org/10.1016/j.neuron.2005.05.020 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bayer J, Bandurski P, Sommer T (2013) Differential modulation of activity related to the anticipation of monetary gains and losses across the menstrual cycle. Eur J Neurosci 38:3519–3526.  https://doi.org/10.1111/ejn.12347 CrossRefPubMedGoogle Scholar
  9. Bayer J, Gläscher J, Finsterbusch J, Schulte LH, Sommer T (2018) Linear and inverted U-shaped dose-response functions describe estrogen effects on hippocampal activity in young women. Nat Commun 9:1220–1212.  https://doi.org/10.1038/s41467-018-03679-x CrossRefPubMedPubMedCentralGoogle Scholar
  10. Becker JB (1990) Direct effect of 17β-estradiol on striatum: sex differences in dopamine release. Synapse 5:157–164.  https://doi.org/10.1002/syn.890050211 CrossRefPubMedGoogle Scholar
  11. Boulware MI, Weick JP, Becklund BR, Kuo SP, Groth RD, Mermelstein PG (2005) Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J Neurosci 25:5066–5078.  https://doi.org/10.1523/JNEUROSCI.1427-05.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Calipari ES, Juarez B, Morel C et al (2017) Dopaminergic dynamics underlying sex-specific cocaine reward. Nat Commun 8:13877.  https://doi.org/10.1038/ncomms13877 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Carr GD, White NM (1986) Anatomical disassociation of amphetamine’s rewarding and aversive effects: An intracranial microinjection study. Psychopharmacology 89:340–346.  https://doi.org/10.1007/BF00174372 CrossRefPubMedGoogle Scholar
  14. Clithero JA, Rangel A (2014) Informatic parcellation of the network involved in the computation of subjective value. Soc Cogn Affect Neurosci 9:1289–1302.  https://doi.org/10.1093/scan/nst106 CrossRefPubMedGoogle Scholar
  15. Cole SL, Robinson MJF, Berridge KC (2018) Optogenetic self-stimulation in the nucleus accumbens: D1 reward versus D2 ambivalence. PLoS One 13:e0207694.  https://doi.org/10.1371/journal.pone.0207694 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cools R (2006) Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson’s disease. Neurosci Biobehav Rev 30:1–23.  https://doi.org/10.1016/j.neubiorev.2005.03.024 CrossRefPubMedGoogle Scholar
  17. Cools R, D’Esposito M (2011) Inverted-U–shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry 69:e113–e125.  https://doi.org/10.1016/j.biopsych.2011.03.028 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cordellini MF, Piazzetta G, Pinto KC, Delattre AM, Matheussi F, Carolino RO, Szawka RE, Anselmo-Franci JA, Ferraz AC (2011) Effect of different doses of estrogen on the nigrostriatal dopaminergic system in two 6-hydroxydopamine-induced lesion models of Parkinson’s disease. Neurochem Res 36:955–961.  https://doi.org/10.1007/s11064-011-0428-z CrossRefPubMedGoogle Scholar
  19. Di Paolo T, Rouillard C, Bédard P (1985) 17β-estradiol at a physiological dose acutely increases dopamine turnover in rat brain. Eur J Pharmacol 117:197–203.  https://doi.org/10.1016/0014-2999(85)90604-1 CrossRefPubMedGoogle Scholar
  20. Diederen KMJ, Ziauddeen H, Vestergaard MD et al (2017) Dopamine modulates adaptive prediction error coding in the human midbrain and striatum. J Neurosci 37:1708–1720.  https://doi.org/10.1523/JNEUROSCI.1979-16.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Diekhof EK, Ratnayake M (2016) Menstrual cycle phase modulates reward sensitivity and performance monitoring in young women: preliminary fMRI evidence. Neuropsychologia 84:70–80.  https://doi.org/10.1016/j.neuropsychologia.2015.10.016 CrossRefPubMedGoogle Scholar
  22. Disshon KA, Dluzen DE (1997) Estrogen as a neuromodulator of MPTP-induced neurotoxicity: effects upon striatal dopamine release. Brain Res 764:9–16.  https://doi.org/10.1016/S0006-8993(97)00418-6 CrossRefPubMedGoogle Scholar
  23. Dreher J-C, Schmidt PJ, Kohn P et al (2007) Menstrual cycle phase modulates reward-related neural function in women. Proc Natl Acad Sci 104:2465–2470.  https://doi.org/10.1073/pnas.0605569104 CrossRefPubMedGoogle Scholar
  24. Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299:1898–1902.  https://doi.org/10.1126/science.1077349 CrossRefPubMedGoogle Scholar
  25. Floresco SB, Ghods-Sharifi S, Vexelman C, Magyar O (2006) Dissociable roles for the nucleus accumbens core and shell in regulating set shifting. J Neurosci 26:2449–2457.  https://doi.org/10.1523/JNEUROSCI.4431-05.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Foster TC (2012) Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging. Hippocampus 22:656–669.  https://doi.org/10.1002/hipo.20935 CrossRefPubMedGoogle Scholar
  27. Frank TC, Kim GL, Krzemien A, Van Vugt DA (2010) Effect of menstrual cycle phase on corticolimbic brain activation by visual food cues. Brain Res 1363:81–92.  https://doi.org/10.1016/j.brainres.2010.09.071 CrossRefPubMedGoogle Scholar
  28. Ghalayani P, Tavangar A, Nilchian F, Khalighinejad N (2013) The comparison of salivary level of estrogen and progesterone in 1st , 2nd and 3rd trimester in pregnant women with and without geographic tongue. Dent Res J (Isfahan) 10:609–612Google Scholar
  29. Gläscher JP, O’Doherty JP (2010) Model-based approaches to neuroimaging: combining reinforcement learning theory with fMRI data. Wiley Interdiscip Rev Cogn Sci 1:501–510.  https://doi.org/10.1002/wcs.57 CrossRefPubMedGoogle Scholar
  30. Gläscher J, Hampton AN, O’Doherty JP (2009) Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb Cortex 19:483–495.  https://doi.org/10.1093/cercor/bhn098 CrossRefPubMedGoogle Scholar
  31. Glimcher PW (2011) Understanding dopamine and reinforcement learning: the dopamine reward prediction error hypothesis. PNAS 108:15647–15654.  https://doi.org/10.1073/pnas.1014269108 CrossRefPubMedGoogle Scholar
  32. Gordon JH (1980) Modulation of apomorphine-induced stereotypy by estrogen: time course and dose response. Brain Res Bull 5:679–682CrossRefGoogle Scholar
  33. Grove-Strawser D, Boulware MI, Mermelstein PG (2010) Membrane estrogen receptors activate the metabotropic glutamate receptors mGluR5 and mGluR3 to bidirectionally regulate CREB phosphorylation in female rat striatal neurons. Neuroscience 170:1045–1055.  https://doi.org/10.1016/j.neuroscience.2010.08.012 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Haber SN, Knutson B (2009) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35:4–26.  https://doi.org/10.1038/npp.2009.129 CrossRefPubMedCentralGoogle Scholar
  35. Hart AS, Rutledge RB, Glimcher PW, Phillips PEM (2014) Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term. J Neurosci 34:698–704.  https://doi.org/10.1523/JNEUROSCI.2489-13.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Holland PW, Welsch RE (1977) Robust regression using iteratively reweighted least-squares. Commun Stat Theory Methods 6:813–827.  https://doi.org/10.1080/03610927708827533 CrossRefGoogle Scholar
  37. Ikemoto S, Panksepp J (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Rev 31:6–41.  https://doi.org/10.1016/S0165-0173(99)00023-5 CrossRefPubMedGoogle Scholar
  38. Ikemoto S, Glazier BS, Murphy JM, McBride WJ (1997) Role of dopamine D1 and D2 receptors in the nucleus accumbens in mediating reward. J Neurosci 17:8580–8587CrossRefGoogle Scholar
  39. Inagaki T, Gautreaux C, Luine V (2010) Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm Behav 58:415–426CrossRefGoogle Scholar
  40. Jacobs E, D’Esposito M (2011) Estrogen shapes dopamine-dependent cognitive processes: implications for women’s health. J Neurosci 31:5286–5293.  https://doi.org/10.1523/JNEUROSCI.6394-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Jocham G, Klein TA, Ullsperger M (2011) Dopamine-mediated reinforcement learning signals in the striatum and ventromedial prefrontal cortex underlie value-based choices. J Neurosci 31:1606–1613.  https://doi.org/10.1523/JNEUROSCI.3904-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Jocham G, Klein TA, Ullsperger M (2014) Differential modulation of reinforcement learning by D2 dopamine and NMDA glutamate receptor antagonism. J Neurosci 34:13151–13162.  https://doi.org/10.1523/JNEUROSCI.0757-14.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Knutson B, Gibbs SEB (2007) Linking nucleus accumbens dopamine and blood oxygenation. Psychopharmacology 191:813–822.  https://doi.org/10.1007/s00213-006-0686-7 CrossRefPubMedGoogle Scholar
  44. Kuhl H (2005) Pharmacology of estrogens and progestogens: influence of different routes of administration. Climacteric 8:3–63.  https://doi.org/10.1080/13697130500148875 CrossRefPubMedGoogle Scholar
  45. Le Saux M, Morissette M, Di Paolo T (2006) ERβ mediates the estradiol increase of D2 receptors in rat striatum and nucleus accumbens. Neuropharmacology 50:451–457.  https://doi.org/10.1016/j.neuropharm.2005.10.004 CrossRefPubMedGoogle Scholar
  46. Levine FM, De Simone LL (1991) The effects of experimenter gender on pain report in male and female subjects. Pain 44:69–72.  https://doi.org/10.1016/0304-3959(91)90149-R CrossRefPubMedGoogle Scholar
  47. Luine VN (2014) Estradiol and cognitive function: past, present and future. Horm Behav 66:602–618.  https://doi.org/10.1016/j.yhbeh.2014.08.011 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Macoveanu J (2014) Serotonergic modulation of reward and punishment: evidence from pharmacological fMRI studies. Brain Res 1556:19–27.  https://doi.org/10.1016/j.brainres.2014.02.003 CrossRefPubMedGoogle Scholar
  49. Macoveanu J, Henningsson S, Pinborg A, Jensen P, Knudsen GM, Frokjaer VG, Siebner HR (2016) Sex-steroid hormone manipulation reduces brain response to reward. Neuropsychopharmacology 41:1057–1065.  https://doi.org/10.1038/npp.2015.236 CrossRefPubMedGoogle Scholar
  50. McLaughlin KJ, Bimonte-Nelson H, Neisewander JL, Conrad CD (2008) Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17β-estradiol effectiveness in altering CA1 spines. Horm Behav 54:386–395.  https://doi.org/10.1016/j.yhbeh.2008.04.010 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ndefo UA, Mosely N (2010) Estradiol valerate and estradiol valerate/dienogest (natazia) tablets. P T 35:614–617PubMedPubMedCentralGoogle Scholar
  52. Nicola SM, Deadwyler SA (2000) Firing rate of nucleus accumbens neurons is dopamine-dependent and reflects the timing of cocaine-seeking behavior in rats on a progressive ratio schedule of reinforcement. J Neurosci 20:5526–5537CrossRefGoogle Scholar
  53. O’Doherty J, Dayan P, Schultz J et al (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304:452–454.  https://doi.org/10.1126/science.1094285 CrossRefPubMedGoogle Scholar
  54. O’Leary P, Boyne P, Flett P et al (1991) Longitudinal assessment of changes in reproductive hormones during normal pregnancy. Clin Chem 37:667–672PubMedGoogle Scholar
  55. Ossewaarde L, van Wingen GA, Kooijman SC, Bäckström T, Fernández G, Hermans EJ (2011) Changes in functioning of mesolimbic incentive processing circuits during the premenstrual phase. Soc Cogn Affect Neurosci 6:612–620.  https://doi.org/10.1093/scan/nsq071 CrossRefPubMedGoogle Scholar
  56. Pasqualini C, Olivier V, Guibert B, Frain O, Leviel V (1995) Acute stimulatory effect of estradiol on striatal dopamine synthesis. J Neurochem 65:1651–1657CrossRefGoogle Scholar
  57. Reimers L, Büchel C, Diekhof EK (2014) How to be patient. The ability to wait for a reward depends on menstrual cycle phase and feedback-related activity. Front Neurosci:8.  https://doi.org/10.3389/fnins.2014.00401
  58. Renner K, Luine V (1986) Analysis of temporal and dose-dependent effects of estrogen on monoamines in brain nuclei. Brain Res 366:64–71.  https://doi.org/10.1016/0006-8993(86)91281-3 CrossRefPubMedGoogle Scholar
  59. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Classical conditioning II: Current research and theory 2:64–99Google Scholar
  60. Rosner W, Hankinson SE, Sluss PM, Vesper HW, Wierman ME (2013) Challenges to the measurement of estradiol: an endocrine society position statement. J Clin Endocrinol Metab 98:1376–1387.  https://doi.org/10.1210/jc.2012-3780 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Satta R, Certa B, He D, Lasek AW (2018) Estrogen receptor β in the nucleus accumbens regulates the rewarding properties of cocaine in female mice. Int J Neuropsychopharmacol 21:382–392.  https://doi.org/10.1093/ijnp/pyx118 CrossRefPubMedGoogle Scholar
  62. Scharfman HE, Hintz TM, Gomez J, Stormes KA, Barouk S, Malthankar-Phatak GH, McCloskey D, Luine VN, Maclusky NJ (2007) Changes in hippocampal function of ovariectomized rats after sequential low doses of estradiol to simulate the preovulatory estrogen surge. Eur J Neurosci 26:2595–2612.  https://doi.org/10.1111/j.1460-9568.2007.05848.x CrossRefPubMedPubMedCentralGoogle Scholar
  63. Schlagenhauf F, Rapp MA, Huys QJM et al (2013) Ventral striatal prediction error signaling is associated with dopamine synthesis capacity and fluid intelligence. Hum Brain Mapp 34:1490–1499.  https://doi.org/10.1002/hbm.22000 CrossRefPubMedGoogle Scholar
  64. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599CrossRefGoogle Scholar
  65. Shughrue PJ, Lane MV, Merchenthaler I (1997) Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J Comp Neurol 388:507–525.  https://doi.org/10.1002/(SICI)1096-9861(19971201)388:4<507::AID-CNE1>3.0.CO;2-6 CrossRefPubMedGoogle Scholar
  66. Sommer T, Richter K, Singer F, Derntl B, Rune GM, Diekhof E, Bayer J (2018) Effects of the experimental administration of oral estrogen on prefrontal functions in healthy young women. Psychopharmacology 235:3465–3477.  https://doi.org/10.1007/s00213-018-5061-y CrossRefPubMedGoogle Scholar
  67. Stauffer WR, Lak A, Schultz W (2014) Dopamine reward prediction error responses reflect marginal utility. Curr Biol 24:2491–2500.  https://doi.org/10.1016/j.cub.2014.08.064 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Stricker R, Eberhart R, Chevailler M-C et al (2006) Establishment of detailed reference values for luteinizing hormone, follicle stimulating hormone, estradiol, and progesterone during different phases of the menstrual cycle on the Abbott ARCHITECT analyzer. Clin Chem Lab Med 44:883–887.  https://doi.org/10.1515/CCLM.2006.160 CrossRefPubMedGoogle Scholar
  69. Suaud-Chagny MF, Chergui K, Chouvet G, Gonon F (1992) Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during local in vivo application of amino acids in the ventral tegmental area. Neuroscience 49:63–72.  https://doi.org/10.1016/0306-4522(92)90076-E CrossRefPubMedGoogle Scholar
  70. Sutton RS, Barto AG (2011) Reinforcement learning: an introductionGoogle Scholar
  71. Thomas J, Météreau E, Déchaud H, Pugeat M, Dreher JC (2014) Hormonal treatment increases the response of the reward system at the menopause transition: a counterbalanced randomized placebo-controlled fMRI study. Psychoneuroendocrinology 50:167–180.  https://doi.org/10.1016/j.psyneuen.2014.08.012 CrossRefPubMedGoogle Scholar
  72. Thompson TL (1999) Attenuation of dopamine uptake in vivo following priming with estradiol benzoate. Brain Res 834:164–167CrossRefGoogle Scholar
  73. Thompson T, Moss R (1994) Estrogen regulation of dopamine release in the nucleus-accumbens: genomic-mediated and nongenomic-mediated effects. J Neurochem 62:1750–1756CrossRefGoogle Scholar
  74. Tobiansky DJ, Will RG, Lominac KD, Turner JM, Hattori T, Krishnan K, Martz JR, Nutsch VL, Dominguez JM (2016) Estradiol in the preoptic area regulates the dopaminergic response to cocaine in the nucleus accumbens. Neuropsychopharmacology 41:1897–1906.  https://doi.org/10.1038/npp.2015.360 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Vehtari A, Gelman A (2014) WAIC and cross-validation in StanGoogle Scholar
  76. Vierk R, Bayer J, Freitag S et al (2015) Structure-function-behavior relationship in estrogen-induced synaptic plasticity. Horm Behav.  https://doi.org/10.1016/j.yhbeh.2015.05.008 CrossRefGoogle Scholar
  77. Yaple ZA, Yu R (2019) Fractionating adaptive learning: a meta-analysis of the reversal learning paradigm. Neurosci Biobehav Rev 102:85–94.  https://doi.org/10.1016/j.neubiorev.2019.04.006 CrossRefPubMedGoogle Scholar
  78. Yarkoni T, Barch DM, Gray JR, Conturo TE, Braver TS (2009) BOLD correlates of trial-by-trial reaction time variability in gray and white matter: a multi-study fMRI analysis. PLoS One 4:e4257.  https://doi.org/10.1371/journal.pone.0004257 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Yoest KE, Cummings JA, Becker JB (2014) Estradiol, dopamine and motivation. Cent Nerv Syst Agents Med Chem 14:83–89CrossRefGoogle Scholar
  80. Yoest KE, Quigley JA, Becker JB (2018) Rapid effects of ovarian hormones in dorsal striatum and nucleus accumbens. Horm Behav.  https://doi.org/10.1016/j.yhbeh.2018.04.002 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Systems NeuroscienceUniversity Medical Center Hamburg-EppendorfHamburgGermany
  2. 2.Department of Basic Psychological Research and Research MethodsUniversity of ViennaViennaAustria

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