The transformation of hormonal stress responses throughout puberty and adolescence.

Prepubertal rats display heightened hormonal stress reactivity compared with adults in that levels of ACTH and corticosterone take twice as long (i.e. 40-60 min) to return to baseline following an acute stressor. Despite this substantial change in stress responsiveness, and the critical nature of the adolescence period of development, the maturation of the hormonal stress response from the time of pubertal onset to adulthood has not been thoroughly investigated. To examine this, we measured ACTH, corticosterone, and testosterone in 30-, 40-, 50-, 60-, and 70-day-old (i.e. spanning pubertal and adolescent development) male rats before and after a 30 min session of restraint stress. We found that the adult-like ACTH stress response develops between 50 and 60 days of age, while the corticosterone response changes between 30 and 40 days of age. We also found that adrenal corticosterone concentrations paralleled the plasma corticosterone response following restraint, suggesting that stress-induced adrenal corticosterone synthesis decreases during adolescent development and may, at least in part, contribute to the differential stress response observed before and after puberty. Finally, stress leads to increases in testosterone secretion, but only after 50 days of age. Collectively, these results indicate that shifts in hormonal stress responses occur throughout adolescent maturation and that these responses show distinct developmental profiles.

[1]  V. A. Padow,et al.  Pubertal‐Related Changes in Hypothalamic‐Pituitary‐Adrenal Axis Reactivity and Cytokine Secretion in Response to an Immunological Stressor , 2011, Journal of neuroendocrinology.

[2]  R. Romeo Adolescence: a central event in shaping stress reactivity. , 2010, Developmental psychobiology.

[3]  R. Romeo Pubertal maturation and programming of hypothalamic–pituitary–adrenal reactivity , 2010, Frontiers in Neuroendocrinology.

[4]  C. McCormick An animal model of social instability stress in adolescence and risk for drugs of abuse , 2010, Physiology & Behavior.

[5]  L. Spear,et al.  Social and non-social anxiety in adolescent and adult rats after repeated restraint , 2009, Physiology & Behavior.

[6]  R. Dahl,et al.  Heightened stress responsiveness and emotional reactivity during pubertal maturation: Implications for psychopathology , 2009, Development and Psychopathology.

[7]  J. Herman,et al.  Estrogen potentiates adrenocortical responses to stress in female rats. , 2007, American journal of physiology. Endocrinology and metabolism.

[8]  R. Viner,et al.  Pubertal transitions in health , 2007, The Lancet.

[9]  C. McCormick,et al.  HPA function in adolescence: Role of sex hormones in its regulation and the enduring consequences of exposure to stressors , 2007, Pharmacology Biochemistry and Behavior.

[10]  Michael K. Skinner,et al.  CHAPTER 38 – Puberty in the Rat , 2006 .

[11]  J. Herman,et al.  Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. , 2006, American journal of physiology. Endocrinology and metabolism.

[12]  J. Ferreira,et al.  Adrenarche in the rat. , 2006, The Journal of endocrinology.

[13]  B. McEwen,et al.  Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor , 2006, Hormones and Behavior.

[14]  B. McEwen,et al.  Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. , 2006, Endocrinology.

[15]  Y. Ulrich‐Lai,et al.  Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[16]  B. McEwen,et al.  Differential Stress Reactivity in Intact and Ovariectomized Prepubertal and Adult Female Rats , 2005, Neuroendocrinology.

[17]  C. Sisk,et al.  The neural basis of puberty and adolescence , 2004, Nature Neuroscience.

[18]  R. Dahl Adolescent Brain Development: A Period of Vulnerabilities and Opportunities. Keynote Address , 2004, Annals of the New York Academy of Sciences.

[19]  B. McEwen,et al.  Testosterone Cannot Activate an Adult-Like Stress Response in Prepubertal Male Rats , 2004, Neuroendocrinology.

[20]  Sarah A. Mustillo,et al.  Prevalence and development of psychiatric disorders in childhood and adolescence. , 2003, Archives of general psychiatry.

[21]  S. Andersen Trajectories of brain development: point of vulnerability or window of opportunity? , 2003, Neuroscience & Biobehavioral Reviews.

[22]  Y. Ulrich‐Lai,et al.  Adrenal Splanchnic Innervation Modulates Adrenal Cortical Responses to Dehydration Stress in Rats , 2002, Neuroendocrinology.

[23]  H. Houshyar,et al.  Marked regulatory shifts in gonadal, adrenal, and metabolic system responses to repeated restraint stress occur within a 3-week period in pubertal male rats. , 2002, Endocrinology.

[24]  V. Viau,et al.  Functional Cross‐Talk Between the Hypothalamic‐Pituitary‐Gonadal and ‐Adrenal Axes , 2002, Journal of neuroendocrinology.

[25]  L. Spear The adolescent brain and age-related behavioral manifestations , 2000, Neuroscience & Biobehavioral Reviews.

[26]  I. Fumal,et al.  Postural Skin Colour Changes during the Corticosteroid Blanching Assay , 1999, Skin Pharmacology and Physiology.

[27]  E. Young,et al.  Sex differences and the HPA axis: implications for psychiatric disease. , 1998, The journal of gender-specific medicine : JGSM : the official journal of the Partnership for Women's Health at Columbia.

[28]  W. Engeland,et al.  Differential Gene Expression of Cytochrome P450 11β-Hydroxylase in Rat Adrenal Cortex after in Vivo Activation. , 1997, Endocrinology.

[29]  V. Viau,et al.  The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  S. Mellon,et al.  P450c11B3 mRNA, Transcribed from a Third P450c11 Gene, Is Expressed in a Tissue-specific, Developmentally, and Hormonally Regulated Fashion in the Rodent Adrenal and Encodes a Protein with Both 11-Hydroxylase and 18-Hydroxylase Activities (*) , 1995, The Journal of Biological Chemistry.

[31]  R. Handa,et al.  Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors , 1994, Physiology & Behavior.

[32]  H. Akil,et al.  Pituitary-Adrenal Response to Ether Vapor in the Weanling Animal: Characterization of the Inhibitory Effect of Glucocorticoids on Adrenocorticotropin Secretion , 1993, Pediatric Research.

[33]  V. Han,et al.  Spatial and temporal distribution of corticosteroid-binding globulin and its messenger ribonucleic acid in embryonic and fetal mice. , 1993, Endocrinology.

[34]  M. Dallman,et al.  Feedback sensitivity of the rat hypothalamo-pituitary-adrenal axis and its capacity to adjust to exogenous corticosterone. , 1992, Endocrinology.

[35]  J. Tresguerres,et al.  Role of LHRH in the gonadotrophin response to restraint stress in intact male rats. , 1990, The Journal of endocrinology.

[36]  J. M. Castellanos,et al.  Effect of acute and chronic stress on testosterone secretion in male rats , 1984, Journal of endocrinological investigation.

[37]  M. Dallman,et al.  Adrenal sensitivity to adrenocorticotropin varies diurnally. , 1981, Endocrinology.

[38]  S. Feldman,et al.  Neural pathways mediating basal and stress-induced secretion of luteinizing hormone, follicle-stimulating hormone, and testosterone in the rat. , 1981, Endocrinology.

[39]  S. Ojeda,et al.  Evidence for changes in sensitivity to testosterone negative feedback on gonadotropin release during sexual development in the male rat. , 1973, Endocrinology.

[40]  S. Schapiro,et al.  Half-life of plasma corticosterone during development. , 1971, Endocrinology.

[41]  V. Viau,et al.  Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat. , 2005, Endocrinology.

[42]  E. Spinedi,et al.  Sex and strain variability in the rat hypothalamo-pituitary-adrenal (HPA) axis function , 1995 .

[43]  J. Meites,et al.  Effects of acute stress on serum LH and prolactin in intact, castrate and dexamethasone-treated male rats. , 1975, Endocrinology.

[44]  S. Levine,et al.  Postweaning development of negative feedback in the pituitary-adrenal system of the rat. , 1973, Neuroendocrinology.