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Stress
The International Journal on the Biology of Stress
Volume 24, 2021 - Issue 5
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Original Research Reports

Age-dependent changes in hormonal stress reactivity following repeated restraint stress throughout adolescence in male rats

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Pages 496-503 | Received 23 Sep 2020, Accepted 05 Jan 2021, Published online: 15 Feb 2021

References

  • Babb, J. A., Masini, C. V., Day, H. E. W., & Campeau, S. (2014). Habituation of hypothalamic-pituitary-adrenocortical axis hormones to repeated homotypic stress and subsequent heterotypic stressor exposure in male and female rats. Stress, 17(3), 224–234. https://doi.org/10.3109/10253890.2014.905534
  • Bhatnagar, S., & Dallman, M. (1998). Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience, 84(4), 1025–1039. https://doi.org/10.1016/s0306-4522(97)00577-0
  • Bhatnagar, S., Huber, R., Nowak, N., & Trotter, P. (2002). Lesions of the posterior paraventricular thalamus block habituation of hypothalamic-pituitary-adrenal responses to repeated restraint. Journal of Neuroendocrinology, 14(5), 403–410. https://doi.org/10.1046/j.0007-1331.2002.00792.x
  • Bingham, B., Gray, M., Sun, T., & Viau, V. (2011). Postnatal blockade of androgen receptors or aromatase impair the expression of stress hypothalamic-pituitary-adrenal axis habituation in adult male rats. Psychoneuroendocrinology, 36(2), 249–257. https://doi.org/10.1016/j.psyneuen.2010.07.015
  • Bingham, B., & Viau, V. (2008). Neonatal gonadectomy and adult testosterone replacement suggest an involvement of limbic arginine vasopressin and androgen receptors in the organization of the hypothalamic-pituitary-adrenal axis. Endocrinology, 149(7), 3581–3591. https://doi.org/10.1210/en.2007-1796
  • Campeau, S., Dolan, D., Akil, H., & Watson, S. J. (2002). c-fos mRNA induction in acute and chronic audiogenic stress: Possible role of the orbitofrontal cortex in habituation. Stress, 5(2), 121–130. https://doi.org/10.1080/10253890290027895
  • Cotella, E. M., Morano, R. L., Wulsin, A. C., Martelle, S. M., Lemen, P., Fitzgerald, M., Packard, B. A., Moloney, R. D., & Herman, J. P. (2020). Lasting impact of chronic adolescent stress and glucocorticoid receptor selective modulation in male and female rats. Psychoneuroendocrinology, 112, 104490 https://doi.org/10.1016/j.psyneuen.2019.104490
  • Dahl, R. E., & Gunnar, M. R. (2009). Heightened stress responsiveness and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology, 21(1), 1–6. https://doi.org/10.1017/S0954579409000017
  • Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2009). Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiology & Behavior, 97(3–4), 484–494. https://doi.org/10.1016/j.physbeh.2009.03.025
  • Foilb, A. R., Lui, P., & Romeo, R. D. (2011). The transformation of hormonal stress responses throughout puberty and adolescence. The Journal of Endocrinology, 210(3), 391–398. https://doi.org/10.1530/JOE-11-0206
  • Goldman, L., Winget, C., Hollingshead, G. W., & Levine, S. (1973). Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology, 12(3), 199–211. https://doi.org/10.1159/000122169
  • Gomez, F., Manalo, S., & Dallman, M. F. (2004). Androgen-sensitive changes in regulation of restraint-induced adrenocorticotropin secretion between early and late puberty in male rats. Endocrinology, 145(1), 59–70. https://doi.org/10.1210/en.2003-0565
  • Gray, M., Bingham, B., & Viau, V. (2010). A comparison of two repeated restraint stress paradigms on hypothalamic-pituitary-adrenal axis habituation, gonadal status and central neuropeptide expression in adult male rats. Journal of Neuroendocrinology, 22(2), 92–101. https://doi.org/10.1111/j.1365-2826.2009.01941.x
  • Green, M. R., Nottrodt, R. E., Simone, J. J., & McCormick, C. M. (2016). Glucocorticoid receptor translocation and expression of relevant genes in the hippocampus of adolescent and adult male rats. Psychoneuroendocrinology, 73, 32–41. https://doi.org/10.1016/j.psyneuen.2016.07.210
  • Grissom, N., & Bhatnagar, S. (2009). Habituation to repeated stress: Get used to it. Neurobiology of Learning and Memory, 92(2), 215–224. https://doi.org/10.1016/j.nlm.2008.07.001
  • Handa, R. J., Kudwa, A. E., Donner, N. C., McGivern, R. F., & Brown, R. (2013). Central 5-alpha reduction of testosterone is required for testosterone's inhibition of the hypothalamo-pituitary-adrenal axis response to restraint stress in adult male rats. Brain Research, 1529, 74–82. https://doi.org/10.1016/j.brainres.2013.07.021
  • Hauger, R. L., Lorang, M., Irwin, M., & Aguilera, G. (1990). CRF receptor regulation and sensitization of ACTH responses to acute ether stress during chronic intermittent immobilization stress. Brain Research, 532(1–2), 34–40. https://doi.org/10.1016/0006-8993(90)91738-3
  • Hodges, T. E., & McCormick, C. M. (2015). Adolescent and adult male rats habituate to repeated isolation, but only adoelscents sensitize to partner familiarity. Hormones and Behavior, 69, 16–30. https://doi.org/10.1016/j.yhbeh.2014.12.003
  • Hueston, C. M., & Deak, T. (2014). On the time course, generality, and regulation of plasma progesterone release in male rats by stress exposure. Endocrinology, 155(9), 3527–3537. https://doi.org/10.1210/en.2014-1060
  • Jackson, M. E., & Moghaddam, B. (2006). Distinct patterns of plasticity in prefrontal cortex neurons that encode slow and fast responses to stress. The European Journal of Neuroscience, 24(6), 1702–1710. https://doi.org/10.1111/j.1460-9568.2006.05054.x
  • Ketelslegers, J. M., Hetzel, W. D., Sherins, R. J., & Catt, K. J. (1978). Developmental changes in testicular gonadotropin receptors: Plasma gonadotropins and plasma testosterone in the rat. Endocrinology, 103(1), 212–222. https://doi.org/10.1210/endo-103-1-212
  • Lee, F. S., Heimer, H., Giedd, J. N., Lein, E. S., Sestan, N., Weinberger, D. R., & Casey, B. J. (2014). Mental health. Adolescent mental health-opportunity and obligation. Science, 346(6209), 547–549. https://doi.org/10.1126/science.1260497
  • Lescoat, G., Lescoat, D., & Garnier, D. H. (1982). Influence of adrenalectomy on maturation of gonadotrophin function in the male rat. The Journal of Endocrinology, 95(1), 1–6. https://doi.org/10.1677/joe.0.0950001
  • Lui, P., Padow, V. A., Franco, D., Hall, B. S., Park, B., Klein, Z. A., & Romeo, R. D. (2012). Divergent stress-induced neuroendocrine and behavioral responses prior to puberty. Physiology & Behavior, 107(1), 104–111. https://doi.org/10.1016/j.physbeh.2012.06.011
  • McCarty, R., & Kopin, I. J. (1979). Stress-induced alterations in plasma catecholamines and behavior of rats: Effects of chlorisondamine and bretylium. Behavioral and Neural Biology, 27(3), 249–265. https://doi.org/10.1016/S0163-1047(79)92314-8
  • McCormick, C. M., Furey, B. F., Child, M., Sawyer, M. J., & Donohue, S. M. (1998). Neonatal sex hormones have 'organizational' effects on the hypothalamic-pituitary-adrenal axis of male rats. Brain Research. Developmental Brain Research, 105(2), 295–307. https://doi.org/10.1016/s0165-3806(97)00155-7
  • McCormick, C. M., & Green, M. R. (2013). From the stressed adolescent to the anxious and depressed adult: Investigations in rodent models. Neuroscience, 249, 242–257. https://doi.org/10.1016/j.neuroscience.2012.08.063
  • McCormick, C. M., Green, M. R., & Simone, J. J. (2017). Translational relevance of rodent models of hypothalamic-pituitary-adrenal function and stressors in adolescence. Neurobiology of Stress, 6, 31–43. https://doi.org/10.1016/j.ynstr.2016.08.003
  • McCormick, C. M., Linkroum, W., Sallinen, B. J., & Miller, N. W. (2002). Peripheral and central sex steroids have differential effects on the HPA axis of male and female rats. Stress, 5(4), 235–247. https://doi.org/10.1080/1025389021000061165
  • McCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010). Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain and Cognition, 72(1), 73–85. https://doi.org/10.1016/j.bandc.2009.06.003
  • Nyhuis, T. J., Masini, C. V., Day, H. E. W., & Campeau, S. (2016). Evidence for the integration of stress-related signals by the rostral posterior hypothalamic nucleus in the regulation of acute and repeated stress-evoked Hypothalamo-Pituitary-Adrenal Response in Rat. The Journal of Neuroscience, 36(3), 795–805. https://doi.org/10.1523/JNEUROSCI.3413-15.2016
  • Patton, G. C., & Viner, R. (2007). Pubertal transitions in health. Lancet, 369(9567), 1130–1139. https://doi.org/10.1016/S0140-6736(07)60366-3
  • Pignatelli, D., Xiao, F., Gouveia, A. M., Ferreira, J. G., & Vinson, G. P. (2006). Adrenarche in the rat. The Journal of Endocrinology, 191(1), 301–308. https://doi.org/10.1677/joe.1.06972
  • Poyrazoglu, S., Bas, F., & Darendeliler, F. (2014). Metabolic syndrome in young people. Current Opinion in Endocrinology, Diabetes, and Obesity, 21(1), 56–63. https://doi.org/10.1097/01.med.0000436414.90240.2c
  • Romeo, R. D. (2018). The metamorphosis of adolescent hormonal stress reactivity: A focus on animal models. Frontiers in Neuroendocrinology, 49, 43–51. https://doi.org/10.1016/j.yfrne.2017.12.003
  • Romeo, R. D., Bellani, R., Karatsoreos, I. N., Chhua, N., Vernov, M., Conrad, C. D., & McEwen, B. S. (2006). Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology, 147(4), 1664–1674. https://doi.org/10.1210/en.2005-1432
  • Romeo, R. D., Bellani, R., & McEwen, B. S. (2005). Stress-induced progesterone secretion and progesterone receptor immunoreactivity in the paraventricular nucleus are modulated by pubertal development in male rats. Stress, 8(4), 265–271. https://doi.org/10.1080/10253890500489320
  • Romeo, R. D., Kaplowitz, E. T., Ho, A., & Franco, D. (2013). The influence of puberty on stress reactivity and forebrain glucocorticoid receptor levels in inbred and outbred strains of male and female mice. Psychoneuroendocrinology, 38(4), 592–596. https://doi.org/10.1016/j.psyneuen.2012.07.019
  • Romeo, R. D., Lee, S. J., Chhua, N., McPherson, C. R., & McEwen, B. S. (2004). Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology, 79(3), 125–132. https://doi.org/10.1159/000077270
  • Romeo, R. D., Lee, S. J., & McEwen, B. S. (2004). Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology, 80(6), 387–393. https://doi.org/10.1159/000084203
  • Romeo, R. D., Minhas, S., Svirsky, S. E., Hall, B. S., Savenkova, M., & Karatsoreos, I. N. (2014). Pubertal shifts in adrenal responsiveness to stress and adrenocorticotropic hormone in male rats. Psychoneuroendocrinology, 42, 146–152. https://doi.org/10.1016/j.psyneuen.2014.01.016
  • Romeo, R. D., Patel, R., Pham, L., & So, V. M. (2016). Adolescence and the ontogeny of the hormonal stress response in male and female rats and mice. Neuroscience and Biobehavioral Reviews, 70, 206–216. https://doi.org/10.1016/j.neubiorev.2016.05.020
  • Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24(4), 417–463. https://doi.org/10.1016/s0149-7634(00)00014-2
  • Ulrich-Lai, Y. M., & Engeland, W. C. (2002). Adrenal splanchnic innervation modulates adrenal cortical responses to dehydration stress in rats. Neuroendocrinology, 76(2), 79–92. https://doi.org/10.1159/000064426
  • Vazquez, D. M., & Akil, H. (1993). Pituitary-adrenal response to ether vapor in the weanling animal: Characterization of the inhibitory effect of glucocorticoids on adrenocorticotropin secretion. Pediatric Research, 34(5), 646–653. https://doi.org/10.1203/00006450-199311000-00017
  • Viau, V. (2002). Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. Journal of Neuroendocrinology, 14(6), 506–513. https://doi.org/10.1046/j.1365-2826.2002.00798.x
  • Viau, V., & Meaney, M. J. (1996). The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. The Journal of Neuroscience, 16(5), 1866–1876. https://doi.org/10.1523/JNEUROSCI.16-05-01866.1996
  • Weinberg, M. S., Johnson, D. C., Bhatt, A. P., & Spencer, R. L. (2010). Medial prefrontal cortex activity can disrupt the expression of stress response habituation. Neuroscience, 168(3), 744–756. https://doi.org/10.1016/j.neuroscience.2010.04.006
  • Williamson, M., Bingham, B., Gray, M., Innala, L., & Viau, V. (2010). The medial preoptic nucleus integrates the central influences of testosterone on the paraventricular nucleus of the hypothalamus and its extended circuitries. The Journal of Neuroscience, 30(35), 11762–11770. https://doi.org/10.1523/JNEUROSCI.2852-10.2010
  • Williamson, M., & Viau, V. (2008). Selective contributions of the medial preoptic nucleus to testosterone-dependant regulation of the paraventricular nucleus of the hypothalamus and the HPA axis. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 295(4), R1020–R1030. https://doi.org/10.1152/ajpregu.90389.2008

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