Menstrual variation in the acute testosterone and cortisol response to laboratory stressors correlate with baseline testosterone fluctuations at a within- and between-person level

References

• Acevedo-Rodriguez, A., Kauffman, A. S., Cherrington, B. D., Borges, C. S., Roepke, T. A., & Laconi, M. (2018). Emerging insights into hypothalamic-pituitary-gonadal axis regulation and interaction with stress signalling. Journal of Neuroendocrinology, 30(10), e12590. https://doi.org/10.1111/jne.12590
   PubMed Web of Science ®Google Scholar
• Al-Dujaili, E. A. S., & Sharp, M. A. (2012). Female salivary testosterone: measurement, challenges and applications steroids. In S. Ostojic (Ed.), From physiology to clinical medicine (pp. 129–167). InTech.
   Google Scholar
• Andreano, J. M., Touroutoglou, A., Dickerson, B., & Barrett, L. F. (2018). Hormonal cycles, brain network connectivity, and windows of vulnerability to affective disorder. Trends in Neurosciences, 41(10), 660–676. https://doi.org/10.1016/j.tins.2018.08.007
   PubMed Web of Science ®Google Scholar
• Baron, R. M., & Kenny, D. A. (1986). The moderator-mediator variable distinction in social psychological research: Conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology, 51(6), 1173–1182. https://doi.org/10.1037//0022-3514.51.6.1173
   PubMed Web of Science ®Google Scholar
• Bateup, H. S., Booth, A., Shirtcliff, E. A., & Granger, D. A. (2002). Testosterone, cortisol, and women’s competition. Evolution and Human Behavior, 23(3), 181–192. https://doi.org/10.1016/S1090-5138(01)00100-3
   Web of Science ®Google Scholar
• Bloch, M., Schmidt, P. J., Su, T. P., Tobin, M. B., & Rubinow, D. R. (1998). Pituitary-adrenal hormones and testosterone across the menstrual cycle in women with premenstrual syndrome and controls. Biological Psychiatry, 43(12), 897–903. https://doi.org/10.1016/s0006-3223(98)00403-x
   PubMed Web of Science ®Google Scholar
• Burger, H. G. (2002). Androgen production in women. Fertility and Sterility, 77(S4), 3–5. https://doi.org/10.1016/S0015-0282(02)02985-0
   Google Scholar
• Casto, K. V., Edwards, D. A., Akinola, M., Davis, C., & Mehta, P. H. (2020). Testosterone reactivity to competition and competitive endurance in men and women. Hormones and Behavior, 123, 104665. https://doi.org/10.1016/j.yhbeh.2019.104665
   PubMed Web of Science ®Google Scholar
• Childs, E., Dlugos, A., & De Wit, H. (2010). Cardiovascular, hormonal, and emotional responses to the TSST in relation to sex and menstrual cycle phase. Psychophysiology, 47(3), 550–559. https://doi.org/10.1111/j.1469-8986.2009.00961.x
   PubMed Web of Science ®Google Scholar
• Chrousos, G. P., Torpy, D. J., & Gold, P. W. (1998). Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: Clinical implications. Annals of Internal Medicine, 129(3), 229–240. https://doi.org/10.7326/0003-4819-129-3-199808010-00012
   PubMedGoogle Scholar
• Collins, A., Eneroth, P., & Landgren, B. M. (1985). Psychoneuroendocrine stress responses and mood as related to the menstrual cycle. Psychosomatic Medicine, 47(6), 512–527. https://doi.org/10.1097/00006842-198511000-00002
   PubMed Web of Science ®Google Scholar
• Cook, C. J., & Crewther, B. T. (2019). Within- and between-person variation in morning testosterone is associated with economic risk-related decisions in athletic women across the menstrual cycle. Hormones and Behavior, 112, 77–80. https://doi.org/10.1016/j.yhbeh.2019.04.007
   PubMed Web of Science ®Google Scholar
• Cook, C. J., Crewther, B. T., & Smith, A. (2012). Comparison of baseline free testosterone and cortisol concentrations between elite and non-elite female athletes. American Journal of Human Biology, 24(6), 856–858. https://doi.org/10.1002/ajhb.22302
   PubMed Web of Science ®Google Scholar
• Cook, C. J., Kilduff, L. P., & Crewther, B. T. (2018). Basal and stress-induced salivary testosterone variation across the menstrual cycle and linkage to motivation and muscle power. Scandinavian Journal of Medicine & Science in Sports, 28(4), 1345–1353. https://doi.org/10.1111/sms.13041
   PubMed Web of Science ®Google Scholar
• Crewther, B. T., & Cook, C. J. (2018a). A longitudinal analysis of salivary testosterone concentrations and competitiveness in elite and non-elite women athletes. Physiology & Behavior, 188, 157–161. https://doi.org/10.1016/j.physbeh.2018.02.012
   PubMed Web of Science ®Google Scholar
• Crewther, B. T., & Cook, C. J. (2018b). The salivary testosterone response to a chance-determined contest is associated with faze-gazing behaviours in athletic women. Hormones and Behavior, 103, 107–110. https://doi.org/10.1016/j.yhbeh.2018.06.011
   PubMed Web of Science ®Google Scholar
• Crewther, B. T., & Cook, C. J. (2019). The digit ratio (2D:4D) relationship with testosterone is moderated by physical training: evidence of prenatal organizational influences on activational patterns of adult testosterone in physically-active women. Early Human Development, 131, 51–55. https://doi.org/10.1016/j.earlhumdev.2019.02.008
   PubMed Web of Science ®Google Scholar
• Crewther, B. T., Hamilton, D., Casto, K., Kilduff, L. P., & Cook, C. J. (2015). Effects of oral contraceptive use on the salivary testosterone and cortisol responses to training sessions and competitions in elite women athletes. Physiology & Behavior, 147, 84–90. https://doi.org/10.1016/j.physbeh.2015.04.017
   PubMed Web of Science ®Google Scholar
• Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130(3), 355–391. https://doi.org/10.1037/0033-2909.130.3.355
   PubMed Web of Science ®Google Scholar
• Edinger, K. L., & Frye, C. A. (2005). Testosterone’s anti-anxiety and analgesic effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus. Psychoneuroendocrinology, 30(5), 418–430. https://doi.org/10.1016/j.psyneuen.2004.11.001
   PubMed Web of Science ®Google Scholar
• Fuss, J., Claro, L., Ising, M., Biedermann, S. V., Wiedemann, K., Stalla, G. K., Briken, P., & Auer, M. K. (2019). Does sex hormone treatment reverse the sex-dependent stress regulation? A longitudinal study on hypothalamus-pituitary-adrenal (HPA) axis activity in transgender individuals. Psychoneuroendocrinology, 104, 228–237. https://doi.org/10.1016/j.psyneuen.2019.02.023
   PubMed Web of Science ®Google Scholar
• Gangestad, S. W., Haselton, M. G., Welling, L. L. M., Gildersleeve, K., Pillsworth, E. G., Burriss, R. P., Larson, C. M., & Puts, D. A. (2016). How valid are assessments of conception probability in ovulatory cycle research? Evaluations, recommendations, and theoretical implications. Evolution and Human Behavior, 37(2), 85–96. https://doi.org/10.1016/j.evolhumbehav.2015.09.001
   Web of Science ®Google Scholar
• Goldstein, J. M., Jerram, M., Abbs, B., Whitfield-Gabrieli, S., & Makris, N. (2010). Sex differences in stress response circuitry activation dependent on female hormonal cycle. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 30(2), 431–438. https://doi.org/10.1523/JNEUROSCI.3021-09.2010
   PubMed Web of Science ®Google Scholar
• Gordon, J. L., & Girdler, S. S. (2014). Mechanisms underlying hemodynamic and neuroendocrine stress reactivity at different phases of the menstrual cycle. Psychophysiology, 51(4), 309–318. https://doi.org/10.1111/psyp.12177
   PubMed Web of Science ®Google Scholar
• Hahn, A. C., Fisher, C. I., Cobey, K. D., DeBruine, L. M., & Jones, B. C. (2016). A longitudinal analysis of women’s salivary testosterone and intrasexual competitiveness. Psychoneuroendocrinology, 64, 117–122. https://doi.org/10.1016/j.psyneuen.2015.11.014
   PubMed Web of Science ®Google Scholar
• Hlavacova, N., Wawruch, M., Tisonova, J., & Jezova, D. (2008). Neuroendocrine activation during combined mental and physical stress in women depends on trait anxiety and the phase of the menstrual cycle. Annals of the New York Academy of Sciences, 1148, 520–525. https://doi.org/10.1196/annals.1410.030
   PubMed Web of Science ®Google Scholar
• Jezova, D., Balagova, L., Chmelova, M., & Hlavacova, N. (2019). Classical steroids in a new fashion: focus on testosterone and aldosterone. Current Protein & Peptide Science, 20(11), 1112–1118. https://doi.org/10.2174/1389203720666190704151254
   PubMed Web of Science ®Google Scholar
• Kanaley, J. A., Boileau, R. A., Bahr, J. M., Misner, J. E., & Nelson, R. A. (1992). Cortisol levels during prolonged exercise: the influence of menstrual phase and menstrual status. International Journal of Sports Medicine, 13(4), 332–336. https://doi.org/10.1055/s-2007-1021276
   PubMed Web of Science ®Google Scholar
• Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999). Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosomatic Medicine, 61(2), 154–162. https://doi.org/10.1097/00006842-199903000-00006
   PubMed Web of Science ®Google Scholar
• Kirschbaum, C., Platte, P., Pirke, K.-M., & Hellhammer, D. I. R. K. (1996). Adrenocortical activation following stressful exercise: Further evidence for attenuated free cortisol responses in women using oral contraceptives. Stress Medicine, 12(3), 137–143. https://doi.org/10.1002/(SICI)1099-1700(199607)12:3<137::AID-SMI685>3.0.CO;2-C
   Google Scholar
• Kroon, J., Pereira, A. M., & Meijer, O. C. (2020). Glucocorticoid sexual dimorphism in metabolism: Dissecting the role of sex hormones. Trends in Endocrinology and Metabolism: TEM, 31(5), 357–367. https://doi.org/10.1016/j.tem.2020.01.010
   PubMed Web of Science ®Google Scholar
• Kudielka, B. M., Hellhammer, D. H., & Wüst, S. (2009). Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology, 34(1), 2–18. https://doi.org/10.1016/j.psyneuen.2008.10.004
   PubMed Web of Science ®Google Scholar
• Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: tests in linear mixed effects models. Journal of Statistical Software, 82(13), 1–26.
   Web of Science ®Google Scholar
• Lane, A. R., O’Leary, C. B., & Hackney, A. C. (2015). Menstrual cycle phase effects free testosterone responses to prolonged aerobic exercise. Acta Physiologica Hungarica, 102(3), 336–341. https://doi.org/10.1556/036.102.2015.3.11
   PubMedGoogle Scholar
• Maki, P. M., Mordecai, K. L., Rubin, L. H., Sundermann, E., Savarese, A., Eatough, E., & Drogos, L. (2015). Menstrual cycle effects on cortisol responsivity and emotional retrieval following a psychosocial stressor. Hormones and Behavior, 74, 201–208. https://doi.org/10.1016/j.yhbeh.2015.06.023
   PubMed Web of Science ®Google Scholar
• Nakamura, Y., Aizawa, K., Imai, T., Kono, I., & Mesaki, N. (2011). Hormonal responses to resistance exercise during different menstrual cycle states. Medicine and Science in Sports and Exercise, 43(6), 967–973. https://doi.org/10.1249/MSS.0b013e3182019774
   PubMed Web of Science ®Google Scholar
• Probst, F., Golle, J., Lory, V., & Lobmaier, J. S. (2018). Reactive aggression tracks within-participant changes in women’s salivary testosterone. Aggressive Behavior, 44(4), 362–371. https://doi.org/10.1002/ab.21757
   PubMed Web of Science ®Google Scholar
• Raudenbush, S. W. & Bryk, A. S. (2002). Hierarchical linear models. Sage.
   Google Scholar
• Roca, C. A., Schmidt, P. J., Altemus, M., Deuster, P., Danaceau, M. A., Putnam, K., & Rubinow, D. R. (2003). Differential menstrual cycle regulation of hypothalamic-pituitary-adrenal axis in women with premenstrual syndrome and controls. The Journal of Clinical Endocrinology and Metabolism, 88(7), 3057–3063. https://doi.org/10.1210/jc.2002-021570
   PubMed Web of Science ®Google Scholar
• Rosnow, R. L., Rosenthal, R., & Rubin, D. B. (2000). Contrasts and correlations in effect-size estimation. Psychological Science, 11(6), 446–453. https://doi.org/10.1111/1467-9280.00287
   PubMed Web of Science ®Google Scholar
• Rubinow, D. R., Roca, C. A., Schmidt, P. J., Danaceau, M. A., Putnam, K., Cizza, G., Chrousos, G., & Nieman, L. (2005). Testosterone suppression of CRH-stimulated cortisol in men. Neuropsychopharmacology, 30(10), 1906–1912. https://doi.org/10.1038/sj.npp.1300742
   PubMed Web of Science ®Google Scholar
• Salonia, A., Pontillo, M., Nappi, R. E., Zanni, G., Fabbri, F., Scavini, M., Daverio, R., Gallina, A., Rigatti, P., Bosi, E., Bonini, P. A., & Montorsi, F. (2008). Menstrual cycle-related changes in circulating androgens in healthy women with self-reported normal sexual function. The Journal of Sexual Medicine, 5(4), 854–863. https://doi.org/10.1111/j.1743-6109.2008.00791.x
   PubMed Web of Science ®Google Scholar
• Shultz, S. J., Wideman, L., Montgomery, M. M., & Levine, B. J. (2011). Some sex hormone profiles are consistent over time in normal menstruating women: implications for sports injury epidemiology. British Journal of Sports Medicine, 45(9), 735–742. https://doi.org/10.1136/bjsm.2009.064931
   PubMed Web of Science ®Google Scholar
• Stanojević, A., Marković, V. M., Maćešić, S., Kolar-Anić, L., & Vukojević, V. (2018). Kinetic modelling of testosterone-related differences in the hypothalamic–pituitary–adrenal axis response to stress. Reaction Kinetics, Mechanisms and Catalysis, 123(1), 17–30. https://doi.org/10.1007/s11144-017-1315-7
   Web of Science ®Google Scholar
• Sung, E., Han, A., Hinrichs, T., Vorgerd, M., Manchado, C., & Platen, P. (2014). Effects of follicular versus luteal phase-based strength training in young women. SpringerPlus, 3(1), 610–618. https://doi.org/10.1186/2193-1801-3-668
   PubMedGoogle Scholar
• Tersman, Z., Collins, A., & Eneroth, P. (1991). Cardiovascular responses to psychological and physiological stressors during the menstrual cycle. Psychosomatic Medicine, 53(2), 185–197. https://doi.org/10.1097/00006842-199103000-00008
   PubMed Web of Science ®Google Scholar
• Viau, V. (2002). Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. Journal of Neuroendocrinology, 14(6), 506–513. https://doi.org/10.1046/j.1365-2826.2002.00798.x
   PubMed Web of Science ®Google Scholar
• Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: When and how. Journal of Neuroendocrinology, 15(8), 711–724. https://doi.org/10.1046/j.1365-2826.2003.01033.x
   PubMed Web of Science ®Google Scholar
• Zavala, E., Voliotis, M., & Zerenner, T. (2020). Dynamic hormone control of stress and fertility. Frontiers in Physiology, 11, 598845. https://doi.org/10.3389/fphys.2020.598845
   PubMed Web of Science ®Google Scholar