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Diurnal Within-Person Coupling Between Testosterone and Cortisol in Healthy Men: Evidence of Positive and Bidirectional Time-Lagged Associations Using a Continuous-Time Model

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Abstract

Objective

The hypothalamic-pituitary-gonadal (HPG) and -adrenal (HPA) axes are traditional viewed as mutually inhibitory systems. However, several diurnal studies have reported positive within-person testosterone and cortisol relationships, as evidence of facilitative processes, but with some constraints (e.g., low-frequency sampling, use of static longitudinal models). Continuous-time (CT) models can help illuminate testosterone-cortisol “coupling” by testing for bidirectional, cross-lagged effects.

Methods

This study investigated diurnal testosterone and cortisol coupling in healthy males (n = 30) using high-frequency sampling protocols. Participants self-collected saliva at work or home using one of three sampling formats; every 10 mins for 9 h, 15 mins for 8 h, and 30 mins for 10 h. After detrending, daily within-person fluctuations in testosterone and cortisol concentration were modeled in a CT framework.

Results

Autoregressive effects for each hormone indicated moderate stability over a shorter period (~6 mins), as a mean-reverting process, and higher stability over longer time periods. Cross-lagged effects were also demonstrated, with testosterone showing a positive relationship to cortisol (.12 within-person standardized effect) and cortisol to testosterone (.08). Both linkages followed a non-linear trajectory, rising in strength from a zero-time lag to peak with a lag of ~8 mins before dissipation beyond this period.

Conclusion

We verified reports of positive within-person coupling between testosterone and cortisol across the day in healthy men. Added novelty comes from bidirectional and time-lagged associations on hormonal pulses, although the effect sizes were small. Hence, we offer a more nuanced understanding of HPG and HPA crosstalk within a CT framework.

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Notes

  1. In a DT framework, auto-effects are termed autoregressive effects and cross-effects are termed cross-lagged effects (Hecht & Voelkle, 2019 provide an overview of DT and CT terminology).

  2. The diffusion matrix can also capture between-person variance, depending on the specified model structure.

References

  • Beaven, M. C., Ingram, J. R., Gill, N. D., & Hopkins, W. G. (2010). Ultradian rhythmicity and induced changes in salivary testosterone. European Journal of Applied Physiology, 110(2), 405–413.

    Article  Google Scholar 

  • Bhake, R., Russell, G. M., Kershaw, Y., Stevens, K., Zaccardi, F., Warburton, V. E. C., et al. (2020). Continuous free cortisol profiles in healthy men: Validation of microdialysis method. Journal of Clinical Endocrinology and Metabolism, 105(4), 1–13.

    Article  Google Scholar 

  • Booij, S. H., Wigman, J. T. W., Jacobs, N., Thiery, E., Derom, C., Wichers, M., & Oravecz, Z. (2020). Cortisol dynamics in depression: Application of a continuous-time process model. Psychoneuroendocrinology, 115, 104598. https://doi.org/10.1016/j.psyneuen.2020.104598.

    Article  Google Scholar 

  • Burger, H. G. (2002). Androgen production in women. Fertility and Sterility, 77(S4), 3–5.

    Article  Google Scholar 

  • Casto, K. V., & Edwards, D. A. (2016). Testosterone, cortisol, and human competition. Hormones and Behavior, 82, 21–37.

    Article  Google Scholar 

  • Cleveland, W. S., Grosse, E., & Shyu, W. M. (1992). Local regression models. In J. M. Chambers & T. J. Hastie (Eds.), Statistical models in S. Pacific Grove, CA: Wadsworth & Brooks/Cole.

    Google Scholar 

  • Crewther, B. T., Hecht, M., Potts, N., Kilduff, L. P., Drawer, S., Marshall, E., & Cook, C. J. (2020). A longitudinal investigation of bidirectional and time-dependent interrelationships between testosterone and training motivation in an elite rugby environment. Hormones and Behavior, 126, 104866. https://doi.org/10.1016/j.yhbeh.2020.104866.

    Article  Google Scholar 

  • Dismukes, A. R., Shirtcliff, E. A., Hanson, J. L., & Pollak, S. D. (2015). Context influences the interplay of endocrine axes across the day. Developmental Psychobiology, 57(6), 731–741.

    Article  Google Scholar 

  • Driver, C. C., Oud, J. H. L., & Voelkle, M. C. (2017). Continuous time structural equation modeling with R package ctsem. Journal of Statistical Software, 77(5), 1–35.

    Article  Google Scholar 

  • Edwards, D. A., & Turan, B. (2020). Within-person coupling of estradiol, testosterone, and cortisol in women athletes. PeerJ, 8, e8402. https://doi.org/10.7717/peerj.8402.

    Article  Google Scholar 

  • Gettler, L. T., McDade, T. W., & Kuzawa, C. W. (2011). Cortisol and testosterone in Filipino young adult men: Evidence for co-regulation of both hormones by fatherhood and relationship status. American Journal of Human Biology, 23(5), 609–620.

    Article  Google Scholar 

  • Harden, K. P., Wrzus, C., Luong, G., Grotzinger, A., Bajbouj, M., Rauers, A., Wagner, G. G., & Riediger, M. (2016). Diurnal coupling between testosterone and cortisol from adolescence to older adulthood. Psychoneuroendocrinology, 73, 79–90.

    Article  Google Scholar 

  • Hecht, M., & Voelkle, M. C. (2021). Continuous-time modeling in prevention research: An illustration. International Journal of Behavioral Development, 45, 19–27. https://doi.org/10.1177/0165025419885026.

  • Hecht, M., Hardt, K., Driver, C. C., & Voelkle, M. C. (2019). Bayesian continuous-time Rasch models. Psychological Methods, 24, 516–537.

    Article  Google Scholar 

  • Kalafatakis, K., Russell, G. M., Harmer, C. J., Munafo, M. R., Marchant, N., Wilson, A., Brooks, J. C., Durant, C., Thakrar, J., Murphy, P., Thai, N. J., & Lightman, S. L. (2018). Ultradian rhythmicity of plasma cortisol is necessary for normal emotional and cognitive responses in man. Proceedings of the National Academy of Sciences of the United States of America, 115(17), E4091–E4100.

    Article  Google Scholar 

  • Knight, E. L., Sarkar, A., Prasad, S., & Mehta, P. H. (2020). Beyond the challenge hypothesis: The emergence of the dual-hormone hypothesis and recommendations for future research. Hormones and Behavior, 123, 104657. https://doi.org/10.1016/j.yhbeh.2019.104657.

    Article  Google Scholar 

  • Lightman, S. L., & Conway-Campbell, B. L. (2010). The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nature Reviews Neuroscience, 11(10), 710–718.

    Article  Google Scholar 

  • Liu, Z., Cappola, A. R., Crofford, L. J., & Guo, W. (2014). Modeling bivariate longitudinal hormone profiles by hierarchical state space models. Journal of the American Statistical Association, 109, 108–118.

    Article  Google Scholar 

  • Marceau, K., Shirtcliff, E. A., Hastings, P. D., Klimes-Dougan, B., Zahn-Waxler, C., Dorn, L. D., & Susman, E. J. (2014). Within-adolescent coupled changes in cortisol with DHEA and testosterone in response to three stressors during adolescence. Psychoneuroendocrinology, 41, 33–45.

    Article  Google Scholar 

  • Marceau, K., Ruttle, P. L., Shirtcliff, E. A., Hastings, P. D., Klimes-Dougan, B., & Zahn-Waxler, C. (2015). Within-person coupling of changes in cortisol, testosterone, and DHEA across the day in adolescents. Developmental Psychobiology, 57(6), 654–669.

    Article  Google Scholar 

  • Mehta, P. H., & Josephs, R. A. (2010). Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis. Hormones and Behavior, 58(5), 898–906.

    Article  Google Scholar 

  • Oud, J. H. L. (2001). Quasi-longitudinal designs in SEM state space modeling. Statistica Neerlandica, 55(2), 200–220.

    Article  Google Scholar 

  • Redhead, D., Cheng, J. T., Driver, C., Foulsham, T., & O’Gorman, R. (2019). On the dynamics of social hierarchy: A longitudinal investigation of the rise and fall of prestige, dominance, and social rank in naturalistic task groups. Evolution and Human Behavior, 40, 222–234.

    Article  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, 1906–1912.

    Article  Google Scholar 

  • Ruttle, P. L., Shirtcliff, E. A., Armstrong, J. M., Klein, M. H., & Essex, M. J. (2015). Neuroendocrine coupling across adolescence and the longitudinal influence of early life stress. Developmental Psychobiology, 57(6), 688–704.

    Article  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.

    Article  Google Scholar 

  • Toufexis, D., Rivarola, M. A., Lara, H., & Viau, V. (2014). Stress and the reproductive axis. Journal of Neuroendocrinology, 26(9), 573–586.

    Article  Google Scholar 

  • Trifonova, S. T., Gantenbein, M., Turner, J. D., & Muller, C. P. (2013). The use of saliva for assessment of cortisol pulsatile secretion by deconvolution analysis. Psychoneuroendocrinology, 38(7), 1090–1101.

    Article  Google Scholar 

  • Turan, B., Tackett, J. L., Lechtreck, M. T., & Browning, W. R. (2015). Coordination of the cortisol and testosterone responses: A dual axis approach to understanding the response to social status threats. Psychoneuroendocrinology, 62, 59–68.

    Article  Google Scholar 

  • Viau, V. (2002). Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. Journal of Neuroendocrinology, 14(6), 506–513.

    Article  Google Scholar 

  • Voelkle, M. C., Oud, J. H., Davidov, E., & Schmidt, P. (2012). An SEM approach to continuous time modeling of panel data: Relating authoritarianism and anomia. Psychological Methods, 17(2), 176–192.

    Article  Google Scholar 

  • Voelkle, M. C., Gische, C., Driver, C. C., & Lindenberger, U. (2018). The role of time in the quest for understanding psychological mechanisms. Multivariate Behavioral Research, 53(6), 782–805.

    Article  Google Scholar 

  • Waite, E., Kershaw, Y., Spiga, F., & Lightman, S. L. (2009). A glucocorticoid sensitive biphasic rhythm of testosterone secretion. Journal of Neuroendocrinology, 21(9), 737–741.

    Article  Google Scholar 

  • Wang, L. P., & Maxwell, S. E. (2015). On disaggregating between-person and within-person effects with longitudinal data using multilevel models. Psychological Methods, 20(1), 63–83.

    Article  Google Scholar 

  • Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: When and how. Journal of Neuroendocrinology, 15(8), 711–724.

    Article  Google Scholar 

  • Zavala, E., Wedgwood, K. C. A., Voliotis, M., Tabak, J., Spiga, F., Lightman, S. L., & Tsaneva-Atanasova, K. (2019). Mathematical modelling of endocrine systems. Trends in Endocrinology and Metabolism, 30(4), 244–257.

    Article  Google Scholar 

  • Zavala, E., Voliotis, M., Zerenner, T., Tabak, J., Walker, J. J., Li, X. F., Terry, J. R., Lightman, S. L., O’Byrne, K., & Tsaneva-Atanasova, K. (2020). Dynamic hormone control of stress and fertility. Frontiers in Physiology, 11, 598845. https://doi.org/10.3389/fphys.2020.598845.

    Article  Google Scholar 

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Crewther, B.T., Hecht, M. & Cook, C.J. Diurnal Within-Person Coupling Between Testosterone and Cortisol in Healthy Men: Evidence of Positive and Bidirectional Time-Lagged Associations Using a Continuous-Time Model. Adaptive Human Behavior and Physiology 7, 89–104 (2021). https://doi.org/10.1007/s40750-021-00162-8

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