Developmental differences in stress responding after repeated underwater trauma exposures in rats

References

• Ardi, Z., Ritov, G., Lucas, M., & Richter-Levin, G. (2014). The effects of a reminder of underwater trauma on behaviour and memory-related mechanisms in the rat dentate gyrus. International Journal of Neuropsychopharmacology, 17, 571–580. doi:10.1017/S1461145713001272
   PubMed Web of Science ®Google Scholar
• Atkinson, H., Wood, S., Kershaw, Y., Bate, E., & Lightman, S. (2006). Diurnal variation in the responsiveness of the hypothalamic-pituitary-adrenal axis of the male rat to noise stress. Journal of Neuroendocrinology, 18, 526–533. doi:10.1111/j.1365-2826.2006.01444.x
   PubMed Web of Science ®Google Scholar
• Bazak, N., Kozlovsky, N., Kaplan, Z., Matar, M., Golan, H., Zohar, J., … Cohen, H. (2009). Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology, 34, 844–858. doi:10.1016/j.psyneuen.2008.12.018
   PubMed Web of Science ®Google Scholar
• Cabrera, O.A., Hoge, C.W., Bliese, P.D., Castro, C.A., & Messer, S.C. (2007). Childhood adversity and combat as predictors of depression and post-traumatic stress in deployed troops. American Journal of Preventive Medicine, 33, 77–82. doi:10.1016/j.amepre.2007.03.019
   PubMed Web of Science ®Google Scholar
• Cohen, H., Liberzon, I., & Richter-Levin, G. (2009). Exposure to extreme stress impairs contextual odour discrimination in an animal model of PTSD. International Journal of Neuropsychopharmacology, 12, 291–303. doi:10.1017/S146114570800919X
   PubMed Web of Science ®Google Scholar
• Coppens, C.M., Siripornmongcolchai, T., Wibrand, K., Alme, M.N., Buwalda, B., de Boer, S.F., … Bramham, C.R. (2011). Social defeat during adolescence and adulthood differentially induce BDNF-regulated immediate early genes. Frontiers in Behavioral Neuroscience, 5, 72. doi:10.3389/fnbeh.2011.00072
   PubMed Web of Science ®Google Scholar
• de Araujo Costa Folha, O.A., Bahia, C.P., de Aguiar, G.P.S., Herculano, A.M., Coelho, N.L.G., de Sousa, M.B.C., … Pereira, A. (2017). Effect of chronic stress during adolescence in prefrontal cortex structure and function. Behavioral and Brain Research, 326, 44–51. doi:10.1016/j.bbr.2017.02.033
   PubMed Web of Science ®Google Scholar
• 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 and Behavior, 97, 484–494. doi:10.1016/j.physbeh.2009.03.025
   PubMed Web of Science ®Google Scholar
• Eiland, L., & Romeo, R.D. (2013). Stress and the developing adolescent brain. Neuroscience, 249, 162–171. doi:10.1016/j.neuroscience.2012.10.048
   PubMed Web of Science ®Google Scholar
• Genovese, R.F., & Dobre, S. (2017). Mitigation of adverse behavioral impact from predator exposure by the nociceptin/orphanin FQ peptide antagonist J-113397 in rats. Behavioral Pharmacology, 28, 521–530. doi:10.1097/FBP.0000000000000329
   PubMed Web of Science ®Google Scholar
• Genovese, R.F., Johnson, C.C., Tobin, C.A., & Gauchan, S. (2014). Multiple presentations reduce the behavioral impact of protected predator exposure in rats. Behavioral Processes, 108, 105–109. doi:10.1016/j.beproc.2014.09.032
   PubMed Web of Science ®Google Scholar
• Hodges, T.E., & McCormick, C.M. (2015). Adolescent and adult male rats habituate to repeated isolation, but only adolescents sensitize to partner unfamiliarity. Hormones and Behavior, 69, 16–30. doi:10.1016/j.yhbeh.2014.12.003
   PubMed Web of Science ®Google Scholar
• Hollis, F., Isgor, C., & Kabbaj, M. (2013). The consequences of adolescent chronic unpredictable stress exposure on brain and behavior. Neuroscience, 249, 232–241. doi:10.1016/j.neuroscience.2012.09.018
   PubMed Web of Science ®Google Scholar
• Horovitz, O., Tsoory, M.M., Hall, J., Jacobson-Pick, S., & Richter-Levin, G. (2012). Post-weaning to pre-pubertal ('juvenile') stress: a model of induced predisposition to stress-related disorders. Neuroendocrinology, 95, 56–64. doi:10.1159/000331393
   PubMed Web of Science ®Google Scholar
• Isgor, C., Kabbaj, M., Akil, H., & Watson, S.J. (2004). Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus, 14, 636–648. doi:10.1002/hipo.10207
   PubMed Web of Science ®Google Scholar
• Jankord, R., Solomon, M.B., Albertz, J., Flak, J.N., Zhang, R., & Herman, J.P. (2011). Stress vulnerability during adolescent development in rats. Endocrinology, 152, 629–638. doi:10.1210/en.2010-0658
   PubMed Web of Science ®Google Scholar
• Kilpatrick, D.G., Ruggiero, K.J., Acierno, R., Saunders, B.E., Resnick, H.S., & Best, C.L. (2003). Violence and risk of PTSD, major depression, substance abuse/dependence, and comorbidity: results from the national survey of adolescents. Journal of Consulting and Clinical Psychology, 71, 692–700. doi:10.1037/0022-006X.71.4.692
   PubMed Web of Science ®Google Scholar
• Luo, X.M., Yuan, S.N., Guan, X.T., Xie, X., Shao, F., & Wang, W.W. (2014). Juvenile stress affects anxiety-like behavior and limbic monoamines in adult rats. Physiology and Behavior, 135, 7–16. doi:10.1016/j.physbeh.2014.05.035
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1016/j.neuroscience.2012.08.063
   PubMed Web of Science ®Google Scholar
• 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, 73–85. doi:10.1016/j.bandc.2009.06.003
   PubMed Web of Science ®Google Scholar
• McCormick, C.M., Merrick, A., Secen, J., & Helmreich, D.L. (2007). Social instability in adolescence alters the central and peripheral hypothalamic-pituitary-adrenal responses to a repeated homotypic stressor in male and female rats. Journal of Neuroendocrinology, 19, 116–126. doi:10.1111/j.1365-2826.2006.01515.x
   PubMed Web of Science ®Google Scholar
• McCormick, C.M., Smith, C., & Mathews, I.Z. (2008). Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behaviral Brain Research, 187, 228–238. doi:10.1016/j.bbr.2007.09.005
   PubMed Web of Science ®Google Scholar
• Moore, N.L., Altman, D.E., Gauchan, S., & Genovese, R.F. (2016). Adulthood stress responses in rats are variably altered as a factor of adolescent stress exposure. Stress, 19, 295–302. doi:10.1080/10253890.2016.1191465
   PubMed Web of Science ®Google Scholar
• Moore, N.L., Gauchan, S., & Genovese, R.F. (2012). Differential severity of anxiogenic effects resulting from a brief swim or underwater trauma in adolescent male rats. Pharmacology, Biochemistry, and Behavior, 102, 264–268. doi:10.1016/j.pbb.2012.05.002
   PubMed Web of Science ®Google Scholar
• Moore, N.L., Gauchan, S., & Genovese, R.F. (2014). Adolescent traumatic stress experience results in less robust conditioned fear and post-extinction fear cue responses in adult rats. Pharmacology Biochemistry and Behavior, 120, 17–24. doi:10.1016/j.pbb.2014.01.011
   PubMed Web of Science ®Google Scholar
• Moore, N.L., Greenleaf, A.L., Acheson, S.K., Wilson, W.A., Swartzwelder, H.S., & Kuhn, C.M. (2010). Role of cannabinoid receptor type 1 desensitization in greater tetrahydrocannabinol impairment of memory in adolescent rats. Journal of Pharmacology and Experimental Therapeutics, 335, 294–301. doi:10.1124/jpet.110.169359
   PubMed Web of Science ®Google Scholar
• Richter-Levin, G. (1998). Acute and long-term behavioral correlates of underwater trauma–potential relevance to stress and post-stress syndromes. Psychiatry Research, 79, 73–83. doi:10.1016/S0165-1781(98)00030-4
   PubMed Web of Science ®Google Scholar
• Ritov, G., Ardi, Z., & Richter-Levin, G. (2014). Differential activation of amygdala, dorsal and ventral hippocampus following an exposure to a reminder of underwater trauma. Frontiers in Behavioral Neuroscience, 8, 18. doi:10.3389/fnbeh.2014.00018
   PubMed Web of Science ®Google Scholar
• Ritov, G., & Richter-Levin, G. (2014). Water associated zero maze: a novel rat test for long term traumatic re-experiencing. Frontiers in Behavioral Neuroscience, 8, 1. doi:10.3389/fnbeh.2014.00001
   PubMed Web of Science ®Google Scholar
• Romeo, R.D. (2010). Pubertal maturation and programming of hypothalamic-pituitary-adrenal reactivity. Frontiers in Neuroendocrinology, 31, 232–240. doi:10.1016/j.yfrne.2010.02.004
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1016/j.neubiorev.2016.05.020
   PubMed Web of Science ®Google Scholar
• Sadler, A.M., & Bailey, S.J. (2016). Repeated daily restraint stress induces adaptive behavioural changes in both adult and juvenile mice. Physiology and Behavior, 167, 313–323. doi:10.1016/j.physbeh.2016.09.014
   PubMed Web of Science ®Google Scholar
• Samtani, M.N., & Jusko, W.J. (2007). Quantification of dexamethasone and corticosterone in rat biofluids and fetal tissue using highly sensitive analytical methods: assay validation and application to a pharmacokinetic study. Biomedical Chromatography, 21, 585–597. doi:10.1002/bmc.788
   PubMed Web of Science ®Google Scholar
• Sood, R., Ritov, G., Richter-Levin, G., & Barki-Harrington, L. (2013). Selective increase in the association of the β2 adrenergic receptor, β Arrestin-1 and p53 with Mdm2 in the ventral hippocampus one month after underwater trauma. Behavioural Brain Research, 240, 26–28. doi:10.1016/j.bbr.2012.11.009
   PubMed Web of Science ®Google Scholar
• Sood, R., Ritov, G., Boltyansky, B., Spector-Chotiner, A., Richter-Levin, G., & Barki-Harrington, L. (2014). Underwater trauma causes a long-term specific increase in the expression of cyclooxygenase-2 in the ventral CA1 of the hippocampus. Pyschoneuroendocrinology, 49, 62–68. doi:10.1016/j.psyneuen.2014.06.015
   PubMed Web of Science ®Google Scholar
• Spear, L.P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417–463. doi:10.1016/S0149-7634(00)00014-2
   PubMed Web of Science ®Google Scholar
• Stone, E.A., & Quartermain, D. (1997). Greater behavioral effects of stress in immature as compared to mature male mice. Physiology and Behavior, 63, 143–145. doi:10.1016/S0031-9384(97)00366-1
   PubMed Web of Science ®Google Scholar
• Tsoory, M., & Richter-Levin, G. (2006). Learning under stress in the adult rat is differentially affected by ‘juvenile’ or ‘adolescent’ stress. The International Journal of Neuropsychopharmacology, 9, 713–728. doi:10.1017/S1461145705006255
   PubMed Web of Science ®Google Scholar
• van der Kolk, B.A., Roth, S., Pelcovitz, D., Sunday, S., & Spinazzola, J. (2005). Disorders of extreme stress: The empirical foundation of a complex adaptation to trauma. Journal of Trauma Stress, 18, 389–399. doi:10.1002/jts.20047
   PubMed Web of Science ®Google Scholar
• Vyas, A., Mitra, R., Shankaranarayana Rao, B.S., & Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience, 22, 6810–6818. doi:20026655
   PubMed Web of Science ®Google Scholar
• Vyas, A., Pillai, A.G., & Chattarji, S. (2004). Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience, 128, 667–673. doi:10.1016/j.neuroscience.2004.07.013
   PubMed Web of Science ®Google Scholar
• Wang, J., Akirav, I., & Richter-Levin, G. (2000). Short-term behavioral and electrophysiological consequences of underwater trauma. Physiology and Behavior, 70, 327–332. doi:10.1016/S0031-9384(00)00274-2
   PubMed Web of Science ®Google Scholar
• Weintraub, A., Singaravelu, J., & Bhatnagar, S. (2010). Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Research, 1343, 83–92. doi:10.1016/j.brainres.2010.04.068
   PubMed Web of Science ®Google Scholar
• Wust, S., Federenko, I.S., van Rossum, E.F., Koper, J.W., & Hellhammer, D.H. (2005). Habituation of cortisol responses to repeated psychosocial stress-further characterization and impact of genetic factors. Psychoneuroendocrinology, 30, 199–211. doi:10.1016/j.psyneuen.2004.07.002
   PubMed Web of Science ®Google Scholar
• Young, E.A., Abelson, J., & Lightman, S.L. (2004). Cortisol pulsatility and its role in stress regulation and health. Frontiers in Neuroendocrinology, 25, 69–76. doi:10.1016/j.yfrne.2004.07.001
   PubMed Web of Science ®Google Scholar
• Zitnik, G.A., Curtis, A.L., Wood, S.K., Arner, J., & Valentino, R.J. (2016). Adolescent social stress produces an enduring activation of the rat locus coeruleus and alters its coherence with the prefrontal cortex. Neuropsychopharmacology, 41, 1376–1385. doi:10.1038/npp.2015.289
   PubMed Web of Science ®Google Scholar