Adolescence and the ontogeny of the hormonal stress response in male and female rats and mice

Abstract

Adolescent development is marked by many changes in neuroendocrine function, resulting in both immediate and long-term influences on an individual’s physiology and behavior. Stress-induced hormonal responses are one such change, with adolescent animals often showing different patterns of hormonal reactivity following a stressor compared with adults. This review will describe the unique ways in which adolescent animals respond to a variety of stressors and how these adolescent-related changes in hormonal responsiveness can be further modified by the sex and previous experience of the individual. Potential central and peripheral mechanisms that contribute to these developmental shifts in stress reactivity are also discussed. Finally, the short- and long-term programming effects of chronic stress exposure during adolescence on later adult hormonal responsiveness are also examined. Though far from a clear understanding of the neurobehavioral consequences of these adolescent-related shifts in stress reactivity, continued study of developmental changes in stress-induced hormonal responses may shed light on the increased vulnerability to physical and psychological dysfunctions that often accompany a stressful adolescence.

Stress and the adolescent brain

“…For these reasons, it is critical to find convergence with animal models (e.g., see Romeo, Patel, Pham, & So, in press, this issue), which can much more precisely define and control the developmental timing of stressors. These cross species endeavors have identified significant concordance across rodent models of laboratory stress and findings in human adolescents who experience real-world stress (Callaghan, Sullivan, Howell, & Tottenham, 2014; Malter Cohen et al, 2013).…”

“…Most likely, the age of greatest impact will vary by domain of functioning. The human literature on developmental timing effects is much more limited than the animal literature for the reasons mentioned above, and probably the most conservative approach at this time is to appreciate that stressors during development have a profound, and usually different or greater, impact on brain function and to leverage translation across the animal literature (see Romeo et al, in press, this issue), which can much more easily control temporal factors associated with stress.…”

“…Although there has been much less research on the effects of concurrent adversity in adolescence (see Romeo et al, in press, this issue, for rodent studies), Casement and colleagues (2014) examined the prospective associations between challenging social situations for girls at 11–12 years old and neural activation during anticipation of reward when they were 15 years old. There was a negative association between ventral striatum response and maternal warmth, suggesting at a minimum that the ventral striatum may respond quite differently to stressors that are experienced during the adolescent period.…”

Involvement of neuronal nitric oxide synthase in cross-sensitization between chronic unpredictable stress and ethanol in adolescent and adult mice

“…In adolescents, corticosterone levels increased from 4.1 ± 1.8 (basal) to 6.02 ± 2.69 (15 min) mg/dL, while in adults the change was from 3.4 ± 0.78 (basal) to 7.35 ± 1.21 (15 min) mg/dL. In fact, adolescents show higher, similar, or lower ACTH and corticosterone responses, depending on the type of stressor (Romeo, Patel, Pham, & So, 2016). nNOS inhibition by 7NI reduced both ethanol sensitization and cross-sensitization with stress, which is in agreement with studies showing that inhibition of nNOS blocks cocaine-induced sensitization and cross-sensitization between cocaine and methamphetamine (Itzhak, 1997), methamphetamine sensitization (Inoue, Arai, Shibata, & Watanabe, 1996), and morphine sensitization (Zarrindast, Askari, Khalilzadeh, & Nouraei, 2006).…”

Sucrose-induced plasticity in the basolateral amygdala in a ‘comfort’ feeding paradigm

“…Importantly, the younger Wistar rats with a history of sucrose intake had a lower corticosterone response to stress that appeared at the 60 min post-stress time point, and the integrated corticosterone response was decreased by ~16%, placing the temporal dynamics and magnitude of the sucrose-induced corticosterone-blunting within the historical range of the adult Long-Evans rats. Prior work has shown that pre-adolescent rats typically have larger and/or prolonged HPA axis responses to stress when compared to adults, with the corticosterone response becoming adult-like at ~30–40 days of age (Gomez et al 2004; McCormick and Mathews 2007; Romeo et al 2016). This may indicate that in the present study, the corticosterone response of the younger Wistar rats reached the adult-like stage prior to restraint testing.…”