Neuroendocrine coupling across adolescence and the longitudinal influence of early life stress

Abstract

Drawing on conceptual models illustrating the advantages of a multisystemic, interactive, developmental approach to understanding development, the present study examines the covariation of stress and sex hormones across the adolescent transition and the effect of early life stress (ELS) on neuroendocrine coupling to gain insight into atypical development. Morning levels of cortisol, testosterone, and dehydroepiandrosterone (DHEA) were assessed at ages 11, 13, and 15; ELS was assessed during the infancy and preschool periods. Hierarchical linear modeling revealed that cortisol-DHEA coupling patterns progressed to tight, positive coupling across adolescence. Cortisol-testosterone coupling was positive at age 11 but became more negative at ages 13 and 15. Exposure to ELS resulted in more adultlike neuroendocrine coupling patterns earlier in life than non-exposed youth; however the effect of ELS on cortisol-testosterone coupling was unique to girls. Results illustrate trajectories of neuroendocrine coupling that may be unique to adolescence. Moderation by ELS suggests that early stress exposure may prompt earlier adultlike neuroendocrine coupling, particularly within girls, which may contribute to early pubertal development.

A dual‐axis approach to understanding neuroendocrine development

“…We hesitated to introduce new jargon to the field, but ended up with this term to emphasize the shared intra-individual nature of HPA-HPG axis communication and the possibility that coupling can be positive or negative. The investigations converge on positive coupling in the special issue (Bobadilla, et al, 2014; Dismukes, et al, 2014; Dismukes, Shirtcliff, Hanson, & Pollak, in press; Han, et al, 2015; Marceau, et al, 2013; Ruttle, et al, 2013). This suggests that coupling is a robust phenomenon and adds insight to other studies which have investigated the interplay between the HPA and HPG axes (Denson, Mehta, & Ho Tan, 2013; Johnson et al, 2013; Marceau, et al, 2014b; Mehta & Josephs, 2010; Zilioli & Watson, 2012, 2013).…”

“…This developmental profile has been appreciated for decades by sex hormone researchers interested in the organizational-activational hypothesis (Goel & Bale, 2008; Romeo, 2003; Schulz, Molenda-Figueira, & Sisk, 2009)and more recently has been described for stress hormones as well (Gunnar, Talge, & Herrera, 2009a; Shirtcliff & Ruttle, 2010) which enter into a juvenile stress hyporesponsive period(Vazquez, 1998). Such a curiously close developmental profile is directly considered by two papers in the special issue (Han, Miller, Cole, Zahn-Waxler, & Hastings, 2015; Ruttle, et al, 2013). Across a much smaller time frame, it is also notable that these axes – like most other steroid endproducts whose pattern of release is controlled centrally by the suprachiasmatic nuclei – both show a circadian rhythm in which hormone levels decline across the daytime hours(Marceau, et al, 2014a).…”

Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation

“…Although the present data suggest that connectivity does not change with age in the PI group, we acknowledge the possibility that maternal deprivation incites early emergence of negative coupling that later changes to positive or nonsignificant coupling. Although cross-sectional data cannot define the trajectory of connectivity over time in the PI group, there is some evidence that prematurely developing phenotypes maintain throughout adulthood following early life stress (49)(50)(51). In addition, it is notable that the negative connectivity observed in PI adolescents is functioning in the same way as in mature adults, with negative connectivity corresponding to lower anxiety (52), providing further evidence of a mature phenotype in adolescence.…”

Coordination of the cortisol and testosterone responses: A dual axis approach to understanding the response to social status threats

“…In a study using multiple manipulated stressors, Marceau et al (2014) also found a positive within-person association (i.e., coupling) between cortisol and testosterone responses for adolescents. These authors-as well as Ruttle et al (2013)-posed the question of whether or not positive coupling of cortisol and testosterone is specific to adolescence, which is a transition period in development with associated increases in cortisol and testosterone levels that are substantial (Romeo, 2005;Gunnar et al, 2009). To the best of our knowledge, no study examined cortisoltestosterone coupling in children, and only one study did so in adults, finding a trend for a positive cortisol-testosterone coupling during a stress task in a unique sample of military veterans in substance use treatment (Bobadilla et al, 2014).…”

“…Several studies examined within-person cortisol-testosterone coupling for adolescents across the day (during normal daily situations), and usually found evidence for positive coupling (Marceau et al, 2013;Ruttle et al, 2013;Dismukes et al, 2014;Johnson et al, 2014). In a study using multiple manipulated stressors, Marceau et al (2014) also found a positive within-person association (i.e., coupling) between cortisol and testosterone responses for adolescents.…”