Unpredictable chronic stress in juvenile or adult rats has opposite effects, respectively, promoting and impairing resilience

References

• Avital A, Richter-Levin G. 2005. Exposure to juvenile stress exacerbates the behavioral consequences of exposure to stress in the adult rat. Int J Neuropsychopharmacol. 8 2: 163–173.
   Google Scholar
• Avital A, Richter-Levin G, Leschiner S, Spanier I, Veenman L, Weizman A, Gavish M. 2001. Acute and repeated swim stress effects on peripheral benzodiazepine receptors in the rat hippocampus, adrenal, and kidney. Neuropsychopharmacology. 25 5: 669–678.
   Google Scholar
• Avital A, Ram E, Maayan R, Weizman A, Richter-Levin G. 2006. Effects of early-life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex. Brain Res Bull. 68 6: 419–424.
   Google Scholar
• Barna I, Bálint E, Baranyi J, Bakos N, Makara GB, Haller J. 2003. Gender-specific effect of maternal deprivation on anxiety and corticotropin-releasing hormone mRNA expression in rats. Brain Res Bull. 15:85–91.
   Google Scholar
• Benetti F, Mello PB, Bonini JS, Monteiro S, Cammarota M, Izquierdo I. 2009. Early postnatal maternal deprivation in rats induces memory deficits in adult life that can be reversed by donepezil and galantamine. Int J Dev Neurosci. 27 1: 59–64.
   Google Scholar
• Bondi CO, Rodriguez G, Gould GG, Frazer A, Morilak DA. 2007. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology. 33 2: 320–331.
   Google Scholar
• Broadhurst PL. 1975. The Maudsley reactive and nonreactive strains of rats: A survey. Behav Gen. 5 4: 299–319.
   Google Scholar
• Ellenbroek BA, Cools AR. 2000. The long-term effects of maternal deprivation depend on the genetic background. Neuropsychopharmacology. 23:99–106.
   PubMed Web of Science ®Google Scholar
• Ferdman N, Murmu RP, Bock J, Braun K, Leshem M. 2007. Weaning age, social isolation, and gender, interact to determine adult explorative and social behavior and dendritic spine morphology in prefrontal cortex of rats. Behav Brain Res. 180:174–182.
   PubMed Web of Science ®Google Scholar
• Huang LT, Holmes GL, Lai MC, Hung PL, Wang CL, Wang TJ, Yang CH, Liou CW, Yang SN. 2002. Maternal deprivation stress exacerbates cognitive deficits in immature rats with recurrent seizures. Epilepsia. 43 10: 1141–1148.
   Google Scholar
• Iwasaki S, Inoue K, Kiriike N, Hikiji K. 2000. Effect of maternal separation on feeding behavior of rats in later life. Phys Behav. 70:551–556.
   Google Scholar
• Jacobson-Pick S, Richter-Levin G. 2010. Differential impact of juvenile stress and corticosterone in juvenility and in adulthood in male and female rats. Behav Brain Res. 214:268–276.
   PubMed Web of Science ®Google Scholar
• Karst H, Joels M. 2003. Effect of chronic stress on synaptic currents in rat hippocampal dentate gyrus neurons. J Neurophysiol. 89 1: 625–633.
   PubMed Web of Science ®Google Scholar
• Kerr MA, Black MM, Krishnakumar A. 2000. Failure to thrive, maltreatment and the behaviour and development of 6-year-old children from low income, urban families: A cumulative risk model. Child Abuse Negl. 24 5: 587–598.
   PubMed Web of Science ®Google Scholar
• Lauder JM. 1988. Neurotransmitters as morphogens. Prog Brain Res. 73:365–387.
   PubMed Web of Science ®Google Scholar
• Lévy F, Melo AI, Galef BGJr, Madden M, Fleming AS. 2003. Complete maternal deprivation affects social, but not spatial, learning in adult rats. Dev Psychobiol. 43 3: 177–191.
   Google Scholar
• Liu D, Caldji C, Sharma S, Plotsky PM, Meaney MJ. 2000. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol. 12 1: 5–12.
   Google Scholar
• Luine V, Villegas M, Martinez C, McEwen BS. 1994. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639 1: 167–170.
   PubMed Web of Science ®Google Scholar
• Mash EJ, Wolfe DA. 2005. Abnormal child psychology. Belmont, CA: Thomson Learning, Wadsworth Publishing.
   Google Scholar
• McAllister TW, Saykin AJ, Flashman LA, Sparling MB, Johnson SC, Guerin SJ, Mamourian AC, Weaver JB, Yanofsky N. 1999. Brain activation during working memory one month after mild traumatic brain injury: A functional MRI study. Neurology. 53 6: 1300–1308.
   PubMed Web of Science ®Google Scholar
• Morris RG. 1984. Development of water maze procedure for studying spatial learning in the rat. J Neurosci Meth. 11:47–60.
   PubMed Web of Science ®Google Scholar
• Oitzl MS, Workel JO, Fluttert M, Frösch F, De Kloet ER. 2000. Maternal deprivation affects behaviour from youth to senescence: Amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur J Neurosci. 12 10: 3771–3780.
   Google Scholar
• Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joëls M, Lucassen PJ, Krugers H. 2010. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J Neurosci. 30 19: 6635–6645.
   PubMed Web of Science ®Google Scholar
• Ossowska G, Danilczuk Z, Klenk-Majewska B, Czajkowski L, Zebrowska-Łupina I. 2004. Antidepressants in chronic unpredictable mild stress (cums)-induced deficit of fighting behavior. Pol J Pharmacol. 56 3: 305–311.
   Google Scholar
• Perry BD. 1997. Incubated in terror: Neurodevelopmental factors in the ‘cycle of violence’. In: Osofsky J. editors. Children, youth and violence: The search for solutions. New York: Guilford Press124–148.
   Google Scholar
• Plotsky PM, Meaney MJ. 1993. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res. 18 3: 195–200.
   PubMedGoogle Scholar
• Raftogianni A, Diamantopoulou A, Miltiadous P, Stamatakis A, Stylianopoulou F. 2010. Neonatal and adolescent experiences interact in determining adult stress coping behaviour. FENS Abstr. 5:113.25.
   Google Scholar
• Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA. 2002. Early maternal deprivation reduces the expression of BDNF and N MDA receptor subunits in rat hippocampus. Mol Psychiatry. 7:609–616.
   PubMed Web of Science ®Google Scholar
• Shors TJ, Foy MR, Levine S, Thompson RF. 1990. Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus. Brain Res Bull. 24 5: 663–667.
   Google Scholar
• Teunis MA, Heijnen CJ, Sluyter F, Bakker JM, Van Dam AM, Hof M, Cools AR, Kavelaars A. 2002. Maternal deprivation of rat pups increases clinical symptoms of experimental autoimmune encephalomyelitis at adult age. J Neuroimmunol. 133 2: 30–38.
   Google Scholar
• Toth E, Avital A, Leshem M, Richter-Levin G, Braun K. Neonatal and juvenile stress induces changes in adult social behavior without affecting cognitive function. Behav Brain Res. 2008a; 190:135–139.
   Google Scholar
• Toth E, Gersner R, Wilf-Yarkoni A, Raizel H, Dar DE, Richter-Levin G, Levit O, Zangen A. Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J Neurochem. 2008b; 107 2: 522–532.
   Google Scholar
• Tsoory M, Richter-Levin G. 2006. Learning under stress in the adult rat is differentially affected by ‘juvenile’ or ‘adolescent’ stress. Int J Neuropsychopharmacol. 9 6: 713–728.
   Google Scholar
• Tsoory M, Cohen H, Richter-Levin G. 2007. Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol. 17:245–256.
   PubMed Web of Science ®Google Scholar
• Vaid RR, Yee BK, Shalev U, Rawlins JN, Weiner I, Feldon J, Totterdell S. 1997. Neonatal nonhandling and in utero prenatal stress reduce the density of NADPH-diaphorase-reactive neurons in the fascia dentata and Ammon's horn of rats. J Neurosci. 17 14: 5599–5609.
   Google Scholar
• Vázquez DM, Bailey C, Dent GW, Okimoto DK, Steffek A, López JF, Levine S. 2006. Brain corticotropin releasing hormone circuits in the developing rat: Effect of maternal deprivation. Brain Res. 1121:83–94.
   PubMed Web of Science ®Google Scholar
• Yann SM, Belzung C, Wim EC. 2006. Effects of unpredictable chronic mild stress on anxiety and depression like behavior in mice. Behav Brain Res. 175:43–50.
   Google Scholar