Abstract
Adolescence is a period of continuous development, including the maturation of endogenous rhythms across systems and timescales. Although, these dynamic changes are well-recognized, their continuous structure and hormonal dependence have not been systematically characterized. Given the well-established link between core body temperature (CBT) and reproductive hormones in adults, we hypothesized that high-resolution CBT can be applied to passively monitor pubertal development and disruption with high fidelity. To examine this possibility, we used signal processing to investigate the trajectory of CBT rhythms at the within-day (ultradian), daily (circadian), and ovulatory timescales, their dependence on estradiol (E2), and the effects of hormonal contraceptives. Puberty onset was marked by a rise in fecal estradiol (fE2), followed by an elevation in CBT and circadian power. This time period marked the commencement of 4-day rhythmicity in fE2, CBT, and ultradian power marking the onset of the estrous cycle. The rise in circadian amplitude was accelerated by E2 treatment, indicating a role for this hormone in rhythmic development. Contraceptive administration in later adolescence reduced CBT and circadian power and resulted in disruption to 4-day cycles that persisted after discontinuation. Our data reveal with precise temporal resolution how biological rhythms change across adolescence and demonstrate a role for E2 in the emergence and preservation of multiscale rhythmicity. These findings also demonstrate how hormones delivered exogenously in a non-rhythmic pattern can disrupt rhythmic development. These data lay the groundwork for a future in which temperature metrics provide an inexpensive, convenient method for monitoring pubertal maturation and support the development of hormone therapies that better mimic and support human chronobiology.
Highlights
Adolescence is a period of rhythmic reorganization during which physiology transitions from a non-reproductive juvenile state into reproductive early adulthood (Sisk and Foster, 2004; Hagenauer et al, 2011; Mohr and Sisk, 2013; Pereira et al, 2019)
FE2 concentrations did not differ between groups from p25 to p31, a baseline period prior to puberty onset (χ2 = 4.48, p = 0.214; Figure 1A)
Intact and Intact + C animals’ Fecal E2 (fE2) concentrations exceeded that of OVX animals (χ2 = 15.9, p = 0.001; p = 0.0134 and p = 0.003, respectively; Figure 1B). This difference was maintained at mid puberty and early adulthood
Summary
Adolescence is a period of rhythmic reorganization during which physiology transitions from a non-reproductive juvenile state into reproductive early adulthood (Sisk and Foster, 2004; Hagenauer et al, 2011; Mohr and Sisk, 2013; Pereira et al, 2019). Rhythmic development occurs at multiple timescales, including within-a-day (ultradian rhythms; URs; Bourguignon, 1988), daily (circadian rhythms; CRs; MacKinnon et al, 1978; Garcia et al, 2001), and multi-day ovulatory cycles in females (ovulatory rhythms; ORs; Vidal, 2017) These rhythms occur across physiological systems, serving to increase the efficiency of signal transduction (Lloyd and Stupfel, 1991; Brodsky and Lloyd, 2008; Walker et al, 2010), temporally segregate incompatible processes (Panda, 2016), synchronize internal systems to the environment (Dibner et al, 2010), and maximize reproductive success (Carlson and Shaw, 2019). This suggests individual rhythmic frequencies may each follow distinct developmental trajectories
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