The adaptive and maladaptive continuum of stress responses – a hippocampal perspective

References

Adamec, R., Hebert, M., Blundell, J., and Mervis, R.F. (2012). Dendritic morphology of amygdala and hippocampal neurons in more and less predator stress responsive rats and more and less spontaneously anxious handled controls. Behav. Brain Res. 226, 133–146.10.1016/j.bbr.2011.09.009Suche in Google Scholar PubMed PubMed Central

Aisa, B., Tordera, R., Lasheras, B., Del Río, J., and Ramírez, M.J. (2007). Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32, 256–266.10.1016/j.psyneuen.2006.12.013Suche in Google Scholar PubMed

Aisa, B., Tordera, R., Lasheras, B., Del Río, J., and Ramírez, M.J. (2008). Effects of maternal separation on hypothalamic-pituitary-adrenal responses, cognition and vulnerability to stress in adult female rats. Neuroscience 154, 1218–1226.10.1016/j.neuroscience.2008.05.011Suche in Google Scholar PubMed

Aisa, B., Elizalde, N., Tordera, R., Lasheras, B., Del Río, J., and Ramírez, M.J. (2009). Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: Implications for spatial memory. Hippocampus 19, 1222–1231.10.1002/hipo.20586Suche in Google Scholar PubMed

Akirav, I. and Richter-Levin, G. (2002). Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 22, 9912–9921.10.1523/JNEUROSCI.22-22-09912.2002Suche in Google Scholar

Akirav, I., Sandi, C., and Richter-Levin, G. (2001). Differential activation of hippocampus and amygdala following spatial learning under stress. Eur. J. Neurosci. 14, 719–725.10.1046/j.0953-816x.2001.01687.xSuche in Google Scholar PubMed

Aleisa, A.M., Alzoubi, K.H., Gerges, N.Z., and Alkadhi, K.A. (2006). Chronic psychosocial stress-induced impairment of hippocampal LTP: Possible role of BDNF. Neurobiol. Dis. 22, 453–462.10.1016/j.nbd.2005.12.005Suche in Google Scholar PubMed

Alfarez, D.N., Karst, H., Velzing, E.H., Joëls, M., and Krugers, H.J. (2008). Opposite effects of glucocorticoid receptor activation on hippocampal CA1 dendritic complexity in chronically stressed and handled animals. Hippocampus 18, 20–28.10.1002/hipo.20360Suche in Google Scholar PubMed

Alfonso, J., Fernández, M.E., Cooper, B., Flugge, G., and Frasch, A.C. (2005). The stress-regulated protein M6a is a key modulator for neurite outgrowth and filopodium/spine formation. Proc. Natl. Acad. Sci. USA 102, 17196–17201.10.1073/pnas.0504262102Suche in Google Scholar PubMed PubMed Central

Amat, J., Baratta, M.V., Paul, E., Bland, S.T., Watkins, L.R., and Maier, S.F. (2005). Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat. Neurosci. 8, 365–371.10.1038/nn1399Suche in Google Scholar PubMed

Amat, J., Paul, E., Zarza, C., Watkins, L.R., and Maier, S.F. (2006). Previous experience with behavioral control over stress blocks the behavioral and dorsal raphe nucleus activating effects of later uncontrollable stress: Role of the ventral medial prefrontal cortex. J. Neurosci. 26, 13264–13272.10.1523/JNEUROSCI.3630-06.2006Suche in Google Scholar

Anacker, C., Cattaneo, A., Luoni, A., Musaelyan, K., Zunszain, P.A., Milanesi, E., Rybka, J., Berry, A., Cirulli, F., Thuret, S., et al. (2013a). Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology 38, 872–883.10.1038/npp.2012.253Suche in Google Scholar

Anacker, C., Cattaneo, A., Musaelyan, K., Zunszain, P.A., Horowitz, M., Molteni, R., Luon, A., Calabrese, F., Tansey, K., Gennarelli, M., et al. (2013b). Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proc. Natl. Acad. Sci. USA 110, 8708–8713.10.1073/pnas.1300886110Suche in Google Scholar

Arriza, J.L., Simerly, R.B., Swanson, L.W., and Evans, R.M. (1988). The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron 1, 887–900.10.1016/0896-6273(88)90136-5Suche in Google Scholar

Atif, F., Yousuf, S., and Agrawal, S.K. (2008). Restraint stress-induced oxidative damage and its amelioration with selenium. Eur. J. Pharmacol. 600, 59–63.10.1016/j.ejphar.2008.09.029Suche in Google Scholar PubMed

Avital, A. and Richter-Levin, G. (2005). Exposure to juvenile stress exacerbates the behavioral consequences of exposure to stress in the adult rat. Int. J. Neuropsychopharmacol. 8, 163–173.10.1017/S1461145704004808Suche in Google Scholar PubMed

Bagot, R.C., van Hasselt, F.N., Champagne, D.L., Meaney, M.J., Krugers, H.J., and Joëls, M. (2009). Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol. Learn. Mem. 92, 292–300.10.1016/j.nlm.2009.03.004Suche in Google Scholar PubMed

Baratta, M.V., Christianson, J.P., Gomez, D.M., Zarza, C.M., Amat, J., Masini, C.V., Watkins, L.R., and Maier, S.F. (2007). Controllable versus uncontrollable stressors bi-directionally modulate conditioned but not innate fear. Neuroscience 146, 1495–1503.10.1016/j.neuroscience.2007.03.042Suche in Google Scholar PubMed PubMed Central

Barha, C.K., Brummelte, S., Lieblich, S.E., and Galea, L.A. (2011). Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 21, 1216–1227.10.1002/hipo.20829Suche in Google Scholar PubMed

Beery, A.K. and Francis, D.D. (2011). Adaptive significance of natural variations in maternal care in rats: A translational perspective. Neurosci. Biobehav. Rev. 35, 1552–1561.10.1016/j.neubiorev.2011.03.012Suche in Google Scholar PubMed PubMed Central

Benekareddy, M., Goodfellow, N.M., Lambe, E.K., and Vaidya, V.A. (2010). Enhanced function of prefrontal serotonin 5-HT₂ receptors in a rat model of psychiatric vulnerability. J. Neurosci. 30, 12138–12150.10.1523/JNEUROSCI.3245-10.2010Suche in Google Scholar

Benekareddy, M., Vadodaria, K.C., Nair, A.R., and Vaidya, V.A. (2011). Postnatal serotonin type 2 receptor blockade prevents the emergence of anxiety behavior, dysregulated stress-induced immediate early gene responses, and specific transcriptional changes that arise following early life stress. Biol. Psychiatry 70, 1024–1032.10.1016/j.biopsych.2011.08.005Suche in Google Scholar

Bessa, J.M., Ferreira, D., Melo, I., Marques, F., Cerqueira, J.J., Palha, J.A., Almeida, O.F., and Sousa, N. (2009). The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol. Psychiatry 14, 764–773.10.1038/mp.2008.119Suche in Google Scholar

Beylin, A.V. and Shors, T.J. (2003). Glucocorticoids are necessary for enhancing the acquisition of associative memories after acute stressful experience. Horm. Behav. 43, 124–131.10.1016/S0018-506X(02)00025-9Suche in Google Scholar

Blank, T., Nijholt, I., Eckart, K., and Spiess, J. (2002). Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: Implications for hippocampus-dependent learning. J. Neurosci. 22, 3788–3794.10.1523/JNEUROSCI.22-09-03788.2002Suche in Google Scholar

Boldrini, M., Santiago, A.N., Hen, R., Dwork, A.J., Rosoklija, G.B., Tamir, H., Arango, V., and John Mann, J. (2013). Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacology 38, 1068–1077.10.1038/npp.2013.5Suche in Google Scholar

Bonne, O., Vythilingam, M., Inagaki, M., Wood, S., Neumeister, A., Nugent, A.C., Snow, J., Luckenbaugh, D.A., Bain, E.E., Drevets, W.C., et al. (2008). Reduced posterior hippocampal volume in posttraumatic stress disorder. J. Clin. Psychiatry 69, 1087–1091.10.4088/JCP.v69n0707Suche in Google Scholar

Bradbury, M.J., Akana, S.F., Cascio, C.S., Levin, N., Jacobson, L., and Dallman, M.F. (1991). Regulation of basal ACTH secretion by corticosterone is mediated by both type I (MR) and type II (GR) receptors in rat brain. J. Steroid Biochem. Mol. Biol. 40, 133–142.10.1016/0960-0760(91)90176-6Suche in Google Scholar

Bredy, T.W., Grant, R.J., Champagne, D.L., and Meaney, M.J. (2003). Maternal care influences neuronal survival in the hippocampus of the rat. Eur. J. Neurosci. 18, 2903–2909.10.1111/j.1460-9568.2003.02965.xSuche in Google Scholar PubMed

Brummelte, S. and Galea, L.A. (2010). Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 168, 680–690.10.1016/j.neuroscience.2010.04.023Suche in Google Scholar PubMed

Brunson, K.L., Kramár, E., Lin, B., Chen, Y., Colgin, L.L., Yanagihara, T.K., Lynch, G., and Baram, T.Z. (2005). Mechanisms of late-onset cognitive decline after early-life stress. J. Neurosci. 25, 9328–9338.10.1523/JNEUROSCI.2281-05.2005Suche in Google Scholar

Buwalda, B., Stubbendorff, C., Zickert, N., and Koolhaas, J.M. (2013). Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: A study on the consequences of social stress in rats. Neuroscience 249, 258–270.10.1016/j.neuroscience.2012.12.050Suche in Google Scholar

Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P.M., and Meaney, M.J. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. USA 95, 5335–5340.10.1073/pnas.95.9.5335Suche in Google Scholar

Caldji, C., Diorio, J., Anisman, H., and Meaney, M.J. (2004). Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice. Neuropsychopharmacology 29, 1344–1352.10.1038/sj.npp.1300436Suche in Google Scholar

Calvo, N., Martijena, I.D., Molina, V.A., and Volosin, M. (1998). Metyrapone pretreatment prevents the behavioral and neurochemical sequelae induced by stress. Brain Res. 800, 227–235.10.1016/S0006-8993(98)00515-0Suche in Google Scholar

Cameron, H.A., Tanapat, P., and Gould, E. (1998). Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 82, 349–354.10.1016/S0306-4522(97)00303-5Suche in Google Scholar

Cazakoff, B.N. and Howland, J.G. (2010). Acute stress disrupts paired pulse facilitation and long-term potentiation in rat dorsal hippocampus through activation of glucocorticoid receptors. Hippocampus 20, 1327–1331.10.1002/hipo.20738Suche in Google Scholar PubMed

Champagne, D.L., Bagot, R.C., van Hasselt, F., Ramakers, G., Meaney, M.J., de Kloet, E.R., Joels, M., and Krugers, H. (2008). Maternal care and hippocampal plasticity: Evidence for experience dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 28, 6037–6045.10.1523/JNEUROSCI.0526-08.2008Suche in Google Scholar PubMed PubMed Central

Chao, H.M., Choo, P.H., and McEwen, B.S. (1989). Glucocorticoid and mineralocorticoid receptor mRNA expression in rat brain. Neuroendocrinology 50, 365–371.10.1159/000125250Suche in Google Scholar PubMed

Chaudhury, S., Aurbach, E.L., Sharma, V., Blandino, P. Jr., Turner, C.A., Watson, S.J., and Akil, H. (2014). FGF2 is a target and a trigger of epigenetic mechanisms associated with differences in emotionality: Partnership with H3K9me3. Proc. Natl. Acad. Sci. USA 111, 11834–11839.10.1073/pnas.1411618111Suche in Google Scholar PubMed PubMed Central

Chen, C.C., Yang, C.H., Huang, C.C., and Hsu, K.S. (2010a). Acute stress impairs hippocampal mossy fiber-CA3 long-term potentiation by enhancing cAMP-specific phosphodiesterase 4 activity. Neuropsychopharmacology 35, 1605–1617.10.1038/npp.2010.33Suche in Google Scholar PubMed PubMed Central

Chen, Y., Rex, C.S., Rice, C.J., Dube, C.M., Gall, C.M., Lynch, G., and Baram, T.Z. (2010b). Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotrophin releasing hormone signaling. Proc. Natl. Acad. Sci. USA 107, 13123–13128.10.1073/pnas.1003825107Suche in Google Scholar PubMed PubMed Central

Chen, Y., Kramár, E.A., Chen, L.Y., Babayan, A.H., Andres, A.L., Gall, C.M., Lynch, G., and Baram, T.Z. (2013). Impairment of synaptic plasticity by the stress mediator CRH involves selective destruction of thin dendritic spines via RhoA signaling. Mol. Psychiatry 18, 485–496.10.1038/mp.2012.17Suche in Google Scholar PubMed PubMed Central

Christian, K.M., Miracle, A.D., Wellman, C.L., and Nakazawa, K. (2011). Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 174, 26–36.10.1016/j.neuroscience.2010.11.033Suche in Google Scholar PubMed PubMed Central

Christiansen, S., Bouzinova, E.V., Palme, R., and Wiborg, O. (2012). Circadian activity of the hypothalamic-pituitary-adrenal axis is differentially affected in the rat chronic mild stress model of depression. Stress 15, 647–657.10.3109/10253890.2011.654370Suche in Google Scholar PubMed

Christianson, J.P., Thompson, B.M., Watkins, L.R., and Maier, S.F. (2009). Medial prefrontal cortical activation modulates the impact of controllable and uncontrollable stressor exposure on a social exploration test of anxiety in the rat. Stress 12, 445–450.10.1080/10253890802510302Suche in Google Scholar PubMed PubMed Central

Cirulli, F., Francia, N., berry, A., Aloe, L., Alleva, S., and Suomi, S.J. (2009). Early life stress as a risk factor for mental health: Role of neurotrophins from rodents to non-human primates. Neurosci. Biobehav. Rev. 33, 578–585.10.1016/j.neubiorev.2008.09.001Suche in Google Scholar PubMed PubMed Central

Cohen, H., Liu, T., Kozlovsky, N., Kaplan, Z., Zohar, J., and Mathé, A.A. (2012). The neuropeptide Y (NPY)-ergic system is associated with behavioral resilience to stress exposure in an animal model of post-traumatic stress disorder. Neuropsychopharmacology 37, 350–363.10.1038/npp.2011.230Suche in Google Scholar PubMed PubMed Central

Cole, J., Costafreda, S.G., McGuffin, P., and Fu, C.H. (2011). Hippocampal atrophy in first episode depression: A meta-analysis of magnetic resonance imaging studies. J. Affect. Disord. 134, 483–487.10.1016/j.jad.2011.05.057Suche in Google Scholar PubMed

Conrad, C.D., LeDoux, J.E., Magariños, A.M., and McEwen, B.S. (1999). Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 113, 902–113.10.1037/0735-7044.113.5.902Suche in Google Scholar

Cordero, M.I., Merino J.J., and Sandi, C. (1998). Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behav. Neurosci. 112, 885–891.10.1037/0735-7044.112.4.885Suche in Google Scholar

Cordero, M.I., Venero, C., Kruyt, N.D., and Sandi, C. (2003). Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm. Behav. 44, 338–345.10.1016/S0018-506X(03)00160-0Suche in Google Scholar

Czeh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., Bartolomucci, A., and Fuchs, E. (2001). Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc. Natl. Acad. Sci. USA 98, 12796–12801.10.1073/pnas.211427898Suche in Google Scholar PubMed PubMed Central

Dagyte, G., Van der Zee, E.A., Postema, F., Luiten, P.G., Den Boer, J.A., Trentani, A., and Meerlo, P. (2009). Chronic but not acute foot-shock stress leads to temporary suppression of cell proliferation in rat hippocampus. Neuroscience 162, 904–913.10.1016/j.neuroscience.2009.05.053Suche in Google Scholar PubMed

Dalle Molle, R., Portella, A.K., Goldani, M.Z., Kapczinski, F.P., Leistner-Segal, S., Salum, G.A., Manfro, G.G., and Silveira, P.P. (2012). Associations between parenting behavior and anxiety in a rodent model and a clinical sample: Relationship to peripheral BDNF levels. Transl. Psychiatry 20, 2:e195.Suche in Google Scholar

Daniels, W.M., Pietersen, C.Y., Carstens, M.E., and Stein, D.J, (2004). Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab. Brain Dis. 19, 3–14.10.1023/B:MEBR.0000027412.19664.b3Suche in Google Scholar

de Quervain, D.J., Roozendaal, B., and McGaugh, J.L. (1998). Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394, 787–790.10.1038/29542Suche in Google Scholar PubMed

de Quervain, D.J., Roozendaal, B., Nitsch, R.M., McGaugh, J.L., and Hock, C. (2000). Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat. Neurosci. 3, 313–314.10.1038/73873Suche in Google Scholar PubMed

de Vasconcellos-Bittencourt, A.P., Vendite, D.A., Nassif, M., Crema, L.M., Frozza, R., Thomazi, A.P., Nieto, F.B., Wofchuk, S., Salbego, C., da Rocha, E.R., et al. (2011). Chronic stress and lithium treatments alter hippocampal glutamate uptake and release in the rat and potentiate necrotic cellular death after oxygen and glucose deprivation. Neurochem. Res. 36, 793–800.10.1007/s11064-011-0404-7Suche in Google Scholar PubMed

Diamond, D.M., Bennett, M.C., Fleshner, M., and Rose, G.M. (1992). Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2, 421–430.10.1002/hipo.450020409Suche in Google Scholar PubMed

Diamond, D.M., Park, C.R., Campbell, A.M., and Woodson, J.C. (2005). Competitive interactions between endogenous LTD and LTP in the hippocampus underlie the storage of emotional memories and stress-induced amnesia. Hippocampus 15, 1006–1025.10.1002/hipo.20107Suche in Google Scholar PubMed

Diniz, L., dos Santos, T.B., Britto, L.R., Céspedes, I.C., Garcia, M.C., Spadari-Bratfisch, R.C., Medalha, C.C., de Castro, G.M., Montesano, F.T., and Viana, M.B. (2013). Effects of chronic treatment with corticosterone and imipramine on fos immunoreactivity and adult hippocampal neurogenesis. Behav. Brain Res. 238, 170–177.10.1016/j.bbr.2012.10.024Suche in Google Scholar

Duman, R.S. and Monteggia, L.M. (2006). A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59, 1116–1127.10.1016/j.biopsych.2006.02.013Suche in Google Scholar

Eiland, L., Ramroop, J., Hill, M.N., Manley, J., and McEwen, B.S. (2012). Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 37, 39–47.10.1016/j.psyneuen.2011.04.015Suche in Google Scholar

Evanson, N.K., Herman, J.P., Sakai, R.R., and Krause, E.G. (2010). Nongenomic actions of adrenal steroids in the central nervous system. J. Neuroendocrinol. 22, 846–861.10.1111/j.1365-2826.2010.02000.xSuche in Google Scholar

Fabricius, K., Wörtwein, G., and Pakkenberg, B. (2008). The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus. Brain Struct. Funct. 212, 403–416.10.1007/s00429-007-0169-6Suche in Google Scholar

Fonager, J., Beedholm, R., Clark, B.F., and Rattan, S.I. (2002). Mild stress-induced stimulation of heat-shock protein synthesis and improved functional ability of human fibroblasts undergoing aging in vitro. Exp Gerontol. 37, 1223–1228.10.1016/S0531-5565(02)00128-6Suche in Google Scholar

Frisone, D.F., Frye, C.A., and Zimmerberg, B. (2002). Social isolation stress during the third week of life has age-dependent effects on spatial learning in rats. Behav. Brain Res. 128, 153–160.10.1016/S0166-4328(01)00315-1Suche in Google Scholar

Gapp, K., Soldado-Magraner, S., Alvarez-Sánchez, M., Bohacek, J., Vernaz, G., Shu, H., Franklin, T.B., Wolfer, D., and Mansuy, I.M. (2014). Early life stress in fathers improves behavioural flexibility in their offspring. Nat. Commun. 5, 5466.10.1038/ncomms6466Suche in Google Scholar PubMed

Ghosh, S., Laxmi, T.R., and Chattarji, S. (2013). Functional connectivity from the amygdala to the hippocampus grows stronger after stress. J. Neurosci. 33, 7234–7244.10.1523/JNEUROSCI.0638-13.2013Suche in Google Scholar PubMed PubMed Central

Giachero, M., Bustos, S.G., Calfa, G., and Molina, V.A. (2013). A BDNF sensitive mechanism is involved in the fear memory resulting from the interaction between stress and the retrieval of an established trace. Learn Mem. 20, 245–255.10.1101/lm.029306.112Suche in Google Scholar PubMed

Goldwater, D.S., Pavlides, C., Hunter, R.G., Bloss, E.B., Hof, P.R., McEwen, B.S., and Morrison, J.H. (2009). Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience 164, 798–808.10.1016/j.neuroscience.2009.08.053Suche in Google Scholar

Goodfellow, N.M., Benekareddy, M., Vaidya, V.A., and Lambe, E.K. (2009). Layer II/III of the prefrontal cortex: Inhibition by the serotonin 5-HT1A receptor in development and stress. J. Neurosci. 29, 10094–10103.10.1523/JNEUROSCI.1960-09.2009Suche in Google Scholar

Gong, Y., Chai, Y., Ding, J.H., Sun, X.L., and Hu, G. (2011). Chronic mild stress damages mitochondrial ultrastructure and function in mouse brain. Neurosci. Lett. 488, 76–80.10.1016/j.neulet.2010.11.006Suche in Google Scholar

Gould, E., McEwen, B.S., Tanapat, P., Galea, L.A., and Fuchs, E. (1997). Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17, 2492–2498.10.1523/JNEUROSCI.17-07-02492.1997Suche in Google Scholar

Grace, L., Hescham, S., Kellaway, L.A., Bugarith, K., and Russell, V.A. (2009). Effect of exercise on learning and memory in a rat model of developmental stress. Metab. Brain Dis. 24, 643–657.10.1007/s11011-009-9162-5Suche in Google Scholar

Heine, V.M., Maslam, S., Zareno, J., Joëls, M., and Lucassen, P.J. (2004). Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur. J. Neurosci. 19, 131–144.10.1046/j.1460-9568.2003.03100.xSuche in Google Scholar

Heine, V.M., Zareno, J., Maslam, S., Joels, M., and Lucassen, P.J. (2005). Chronic stress in the adult dentate gyrus reduces cell proliferation near the vasculature and VEGF and Flk-1 protein expression. Eur. J. Neurosci. 21, 1304–1314.10.1111/j.1460-9568.2005.03951.xSuche in Google Scholar

Herman, J.P. and Cullinan, W.E. (1997). Neurocircuitry of stress: Central control of the hypothalamopituitary-adrenocortical axis. Trends Neurosci. 20, 78–84.10.1016/S0166-2236(96)10069-2Suche in Google Scholar

Herman, J.P. and Spencer, R. (1998). Regulation of hippocampal glucocorticoid receptor gene transcription and protein expression in vivo. J. Neurosci. 18, 7462–7473.10.1523/JNEUROSCI.18-18-07462.1998Suche in Google Scholar

Herpfer, I., Hezel, H., Reichardt, W., Clark, K., Geiger, J., Gross, C.M., Heyer, A., Neagu, V., Bhatia, H., Atas, H.C., et al. (2012). Early life stress differentially modulates distinct forms of brain plasticity in young and adult mice. PLoS One 7, e46004.10.1371/journal.pone.0046004Suche in Google Scholar PubMed PubMed Central

Hillerer, K.M., Neumann, I.D., Couillard-Despres, S., Aigner, L., and Slattery, D.A. (2013). Sex-dependent regulation of hippocampal neurogenesis under basal and chronic stress conditions in rats. Hippocampus 23, 476–487.10.1002/hipo.22107Suche in Google Scholar

Holderbach, R., Clark, K., Moreau, J.L., Bischofberger, J., and Normann, C. (2007). Enhanced long-term synaptic depression in an animal model of depression. Biol. Psychiatry 62, 92–100.10.1016/j.biopsych.2006.07.007Suche in Google Scholar

Holmes, A. and Wellman, C.L. (2009). Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci. Biobehav. Rev. 33, 773–783.10.1016/j.neubiorev.2008.11.005Suche in Google Scholar

Howland, J.G. and Wang, Y.T. (2008). Synaptic plasticity in learning and memory: Stress effects in the hippocampus. Prog. Brain Res. 169, 145–158.10.1016/S0079-6123(07)00008-8Suche in Google Scholar

Hu, H., Real, E., Takamiya, K., Kang, M.G., Ledoux, J., Huganir, R.L., and Malinow R. (2007). Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 131, 160–173.10.1016/j.cell.2007.09.017Suche in Google Scholar

Hulshof, H.J., Novati, A., Sgoifo, A., Luiten, P.G., den Boer, J.A., and Meerlo, P. (2011). Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats. Behav. Brain Res. 216, 552–560.10.1016/j.bbr.2010.08.038Suche in Google Scholar

Huot, R.L., Plotsky, P.M., Lenox, R.H., and McNamara, R.K. (2002). Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res. 950, 52–63.10.1016/S0006-8993(02)02985-2Suche in Google Scholar

Isgor, C., Kabbaj, M., Akil, H., and 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, 636–648.10.1002/hipo.10207Suche in Google Scholar PubMed

Ivy, A.S., Rex, C.S., Chen, Y., Dubé, C., Maras, P.M., Grigoriadis, D.E., Gall, C.M., Lynch, G., and Baram, T.Z. (2010). Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J. Neurosci. 30, 13005–13015.10.1523/JNEUROSCI.1784-10.2010Suche in Google Scholar PubMed PubMed Central

Jafari, M., Seese, R.R., Babayan, A.H., Gall, C.M., and Lauterborn, J.C. (2012). Glucocorticoid receptors are localized to dendritic spines and influence local actin signaling. Mol. Neurobiol. 46, 304–315.10.1007/s12035-012-8288-3Suche in Google Scholar PubMed PubMed Central

Jakovcevski, M., Schachner, M., and Morellini, F. (2011). Susceptibility to the long-term anxiogenic effects of an acute stressor is mediated by the activation of the glucocorticoid receptors. Neuropharmacology 61, 1297–1305.10.1016/j.neuropharm.2011.07.034Suche in Google Scholar

Jankord, R. and Herman, J.P. (2008). Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann. N.Y. Acad. Sci. 1148, 64–73.10.1196/annals.1410.012Suche in Google Scholar

Ježek, K., Lee, B.B., Kelemen, E., McCarthy, K.M., McEwen, B.S., and Fenton, A.A. (2010). Stress-induced out-of-context activation of memory. PLoS Biol. 8, e1000570.10.1371/journal.pbio.1000570Suche in Google Scholar

Joels M. (2001). Corticosteroid actions in the hippocampus. J. Neuroendocrinol. 13, 657–669.10.1046/j.1365-2826.2001.00688.xSuche in Google Scholar

Joels, M. and de Kloet, E.R. (1989). Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. Science 245, 1502–1505.10.1126/science.2781292Suche in Google Scholar

Joels, M., Pu, Z., Wiegert, O., Oitzl, M.S., and Krugers, H.J. (2006). Learning under stress: How does it work? Trends Cogn. Sci. 10, 152–158.Suche in Google Scholar

Kalinichev, M., Easterling, K.W., Plotsky, P.M., and Holtzman, S.G. (2002). Long-lasting changes in stress induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol. Biochem. Behav. 73, 131–140.10.1016/S0091-3057(02)00781-5Suche in Google Scholar

Kallarackal, A.J., Kvarta, M.D., Cammarata, E., Jaberi, L., Cai, X., Bailey, A.M., and Thompson, S.M. (2013). Chronic stress induces a selective decrease in AMPA receptor-mediated synaptic excitation at hippocampal temporoammonic-CA1 synapses. J. Neurosci. 33, 15669–15674.10.1523/JNEUROSCI.2588-13.2013Suche in Google Scholar PubMed PubMed Central

Kavushansky, A., Vouimba, R.M., Cohen, H., and Richter-Levin, G. (2006). Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress. Hippocampus 16, 35–42.10.1002/hipo.20130Suche in Google Scholar PubMed

Kim, J.J., Foy, M.R., and Thompson, R.F. (1996). Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc. Natl. Acad. Sci. USA 93, 4750–4753.10.1073/pnas.93.10.4750Suche in Google Scholar PubMed PubMed Central

Kim, J.J., Koo, J.W., Lee, H.J., and Han, J.S. (2005). Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J. Neurosci. 25, 1532–1539.10.1523/JNEUROSCI.4623-04.2005Suche in Google Scholar PubMed PubMed Central

Kippin, T.E., Martens, D.J., and van der Kooy. D. (2005). p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 19, 756–767.10.1101/gad.1272305Suche in Google Scholar PubMed PubMed Central

Kirby, E.D., Muroy, S.E., Sun, W.G., Covarrubias, D., Leong, M.J., Barchas, L.A., and Kaufer, D. (2013). Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2. eLife 16, 2:e00362.Suche in Google Scholar

Kitagawa. K. (2012). Ischemic tolerance in the brain: Endogenous adaptive machinery against ischemic stress. J. Neurosci. Res. 90, 1043–1054.10.1002/jnr.23005Suche in Google Scholar PubMed

Kitchener, P., Di Blasi, F., Borrelli, E., and Piazza, P.V. (2004). Differences between brain structures in nuclear translocation and DNA binding of the glucocorticoid receptor during stress and the circadian cycle. Eur. J. Neurosci. 19, 1837–1846.10.1111/j.1460-9568.2004.03267.xSuche in Google Scholar PubMed

Koehl, M., van der Veen, R., Gonzales, D., Piazza, P.V., and Abrous, D.N. (2012). Interplay of maternal care and genetic influences in programming adult hippocampal neurogenesis. Biol. Psychiatry 72, 282–289.10.1016/j.biopsych.2012.03.001Suche in Google Scholar PubMed

Koide, T., Wieloch, T.W., and Siesjo, B.K. (1986). Chronic dexamethasone pretreatment aggravates ischemic neuronal necrosis. J. Cereb. Blood Flow Metab. 6, 395–404.10.1038/jcbfm.1986.72Suche in Google Scholar PubMed

Koike, H., Ibi, D., Mizoguchi, H., Nagai, T., Nitta, A., Takuma, K., Nabeshima, T., Yoneda, Y., and Yamada, K. (2009). Behavioral abnormality and pharmacologic response in social isolation-reared mice. Behav. Brain Res. 202, 114–121.10.1016/j.bbr.2009.03.028Suche in Google Scholar PubMed

Komatsuzaki, Y., Hatanaka, Y., Murakami, G., Mukai, H., Hojo, Y., Saito, M., Kimoto, T., and Kawato, S. (2012). Corticosterone induces rapid spinogenesis via synaptic glucocorticoid receptors and kinase networks in hippocampus. PLoS One 7, e34124.10.1371/journal.pone.0034124Suche in Google Scholar PubMed PubMed Central

Kompagne, H., Bárdos, G., Szénási, G., Gacsályi, I., Hársing, L.G., and Lévay, G. (2008). Chronic mild stress generates clear depressive but ambiguous anxiety-like behaviour in rats. Behav. Brain. Res. 193, 311–314.10.1016/j.bbr.2008.06.008Suche in Google Scholar PubMed

Koo, J.W. and Duman, R.S. (2008). IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA 105, 751–756.10.1073/pnas.0708092105Suche in Google Scholar PubMed PubMed Central

Koo, J.W., Russo, S.J., Ferguson, D., Nestler, E.J., and Duman, R.S. (2010). Nuclear factor-kappaB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc. Natl. Acad. Sci. USA 107, 2669–2674.10.1073/pnas.0910658107Suche in Google Scholar PubMed PubMed Central

Korosi, A., Shanabrough, M., McClelland, S., Liu, Z.W., Borok, E., Gao, X.B., Horvath, T.L., and Baram, T.Z. (2010). Early-life experience reduces excitation to stress-responsive hypothalamic neurons and reprograms the expression of corticotropin-releasing hormone. J. Neurosci. 30, 703–713.10.1523/JNEUROSCI.4214-09.2010Suche in Google Scholar PubMed PubMed Central

Korz, V. and Frey, J.U. (2003). Stress-related modulation of hippocampal long-term potentiation in rats: Involvement of adrenal steroid receptors. J. Neurosci. 23, 7281–7287.10.1523/JNEUROSCI.23-19-07281.2003Suche in Google Scholar

Koutmani, Y., Politis, P.K., Elkouris, M., Agrogiannis, G., Kemerli, M., Patsouris, E., Remboutsika, E., and Karalis, K.P. (2013). Corticotropin-releasing hormone exerts direct effects on neuronal progenitor cells: Implications for neuroprotection. Mol. Psychiatry 18, 300–307.10.1038/mp.2012.198Suche in Google Scholar PubMed PubMed Central

Kozlovsky, N., Zohar, J., Kaplan, Z., and Cohen, H. (2012). Microinfusion of a corticotrophin-releasing hormone receptor 1 antisense oligodeoxynucleotide into the dorsal hippocampus attenuates stress responses at specific times after stress exposure. J. Neuroendocrinol. 24, 489–503.10.1111/j.1365-2826.2011.02267.xSuche in Google Scholar PubMed

Kubala, K.H., Christianson, J.P., Kaufman, R.D., Watkins, L.R., and Maier, S.F. (2012). Short- and long-term consequences of stressor controllability in adolescent rats. Behav. Brain Res. 234, 278–284.10.1016/j.bbr.2012.06.027Suche in Google Scholar PubMed PubMed Central

Ladd, C.O., Huot, R.L., Thrivikraman, K.V., Nemeroff, C.B., and Plotsky, P.M. (2004). Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol. Psychiatry 55, 367–375.10.1016/j.biopsych.2003.10.007Suche in Google Scholar PubMed

Ladd, C.O., Thrivikraman, K.V., Huot, R.L., and Plotsky, P.M. (2005). Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 30, 520–533.10.1016/j.psyneuen.2004.12.004Suche in Google Scholar PubMed

Lagace, D.C., Donovan, M.H., DeCarolis, N.A., Farnbauch, L.A., Malhotra, S., Berton, O., Nestler, E.J., Krishnan, V., and Eisch, A.J. (2010). Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. Proc. Natl. Acad. Sci. USA 107, 4436–4441.10.1073/pnas.0910072107Suche in Google Scholar PubMed PubMed Central

Lajud, N., Roque, A., Cajero, M., Gutiérrez-Ospina, G., and Torner, L. (2012). Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood. Psychoneuroendocrinology 37, 410–420.10.1016/j.psyneuen.2011.07.011Suche in Google Scholar PubMed

Lee, E. and Son, H. (2009). Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep. 42, 239–244.10.5483/BMBRep.2009.42.5.239Suche in Google Scholar

Lee, K.J., Kim, S.J., Kim, S.W., Choi, S.H., Shin, Y.C., Park, S.H., Moon, B.H., Cho, E., Lee, M.S., Choi, S.H., et al. (2006). Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp. Mol. Med. 38, 44–54.10.1038/emm.2006.6Suche in Google Scholar

Lee, A.G., Buckmaster, C.L., Yi, E., Schatzberg, A.F., and Lyons, D.M. (2014). Coping and glucocorticoid receptor regulation by stress inoculation. Psychoneuroendocrinology 9, 272–279.10.1016/j.psyneuen.2014.07.020Suche in Google Scholar

Lehmann, J., Pryce, C.R., Bettschen, D., and Feldon, J. (1999). The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 64, 705–715.10.1016/S0091-3057(99)00150-1Suche in Google Scholar

Leslie, A.T., Akers, K.G., Krakowski, A.D., Stone, S.S., Sakaguchi, M., Arruda-Carvalho, M., and Frankland, P.W. (2011). Impact of early adverse experience on complexity of adult-generated neurons. Transl. Psychiatry 1, e35.10.1038/tp.2011.38Suche in Google Scholar PubMed PubMed Central

Leuner, B. and Shors, T.J. (2013). Stress, anxiety, and dendritic spines: What are the connections? Neuroscience 251, 108–119.10.1016/j.neuroscience.2012.04.021Suche in Google Scholar PubMed

Li, Z. and Richter-Levin, G. (2012). Stimulus intensity-dependent modulations of hippocampal long-term potentiation by basolateral amygdala priming. Front Cell. Neurosci. 6, 21.10.3389/fncel.2012.00021Suche in Google Scholar PubMed PubMed Central

Lin, Y., Westenbroek, C., Bakker, P., Termeer, J., Liu, A., Li, X., and Ter Horst, G.J. (2008). Effects of long-term stress and recovery on the prefrontal cortex and dentate gyrus in male and female rats. Cereb. Cortex 18, 2762–2774.10.1093/cercor/bhn035Suche in Google Scholar PubMed

Lippmann, M., Bress, A., Nemeroff, C.B., Plotsky, P.M., and Monteggia, L.M. (2007). Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur. J. Neurosci. 25, 3091–3098.10.1111/j.1460-9568.2007.05522.xSuche in Google Scholar PubMed

Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P.M., and Meaney, M.J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659–1662.10.1126/science.277.5332.1659Suche in Google Scholar PubMed

Liu, X., Betzenhauser, M.J., Reiken, S., Meli, A.C., Xie, W., Chen, B.X., Arancio, O., and Marks, A.R. (2012). Role of leaky neuronal ryanodine receptors in stress-induced cognitive dysfunction. Cell 150, 1055–1067.10.1016/j.cell.2012.06.052Suche in Google Scholar PubMed PubMed Central

Lloyd, R.B. and Nemeroff, C.B. (2011). The role of corticotropin-releasing hormone in the pathophysiology of depression: Therapeutic implications. Curr. Top Med. Chem. 11, 609–617.10.2174/1568026611109060609Suche in Google Scholar

Loi, M., Koricka, S., Lucassen, P.J., and Joels, M. (2014). Age- and sex-dependent effects of early life stress on hippocampal neurogenesis. Front. Endocrinol. (Lausanne) 20, 5–13.10.3389/fendo.2014.00013Suche in Google Scholar

Lopez-Duran, N.L., Kovacs, M., and George, C.J. (2009). Hypothalamic-pituitary-adrenal axis dysregulation in depressed children and adolescents: A meta-analysis. Psychoneuroendocrinology 34, 1272–1283.10.1016/j.psyneuen.2009.03.016Suche in Google Scholar

Lowy, M.T., Gault, L., and Yamamoto, B.K. (1993). Adrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J. Neurochem. 61, 1957–1960.10.1111/j.1471-4159.1993.tb09839.xSuche in Google Scholar

Lucassen, P.J., Vollmann-Honsdorf, G.K., Gleisberg, M., Czéh, B., De Kloet, E.R., and Fuchs, E. (2001). Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur. J. Neurosci. 14, 161–166.10.1046/j.0953-816x.2001.01629.xSuche in Google Scholar

Luine, V., Villegas, M., Martinez, C., and McEwen, B.S. (1994). Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639, 167–170.10.1016/0006-8993(94)91778-7Suche in Google Scholar

Lupien, S.J., McEwen, B.S., Gunnar, M.R., and Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behavior and cognition. Nat. Rev. Neurosci. 10, 434–445.10.1038/nrn2639Suche in Google Scholar PubMed

Lyons, D.M., Buckmaster, P.S., Lee, A.G., Wu, C., Mitra, R., Duffey, L.M., Buckmaster, C.L., Her, S., Patel, P.D., and Schatzberg, A.F. (2010). Stress coping stimulates hippocampal neurogenesis in adult monkeys. Proc. Natl. Acad. Sci. USA 107, 14823–14827.10.1073/pnas.0914568107Suche in Google Scholar PubMed PubMed Central

Ma, X.C., Jiang, D., Jiang, W.H., Wang, F., Jia, M., Wu, J., Hashimoto, K., Dang, Y.H., and Gao, C.G. (2011). Social isolation-induced aggression potentiates anxiety and depressive-like behavior in male mice subjected to unpredictable chronic mild stress. PLoS One 6, e20955.10.1371/journal.pone.0020955Suche in Google Scholar PubMed PubMed Central

Macrì, S., Granstrem, O., Shumilina, M., Antunes Gomes dos Santos, F.J., Berry, A., Saso, L., and Laviola, G. (2009). Resilience and vulnerability are dose-dependently related to neonatal stressors in mice. Horm. Behav. 56, 391–398.10.1016/j.yhbeh.2009.07.006Suche in Google Scholar PubMed

Magariños, A.M. and McEwen, B.S. (1995). Stress-induced atrophy of apical dendrites of hippocampal CA3 neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69, 89–98.10.1016/0306-4522(95)00259-LSuche in Google Scholar

Magariños, A.M., McEwen, B.S., Flugge, G., and Fuchs, E. (1996). Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J. Neurosci. 16, 3534–3540.10.1523/JNEUROSCI.16-10-03534.1996Suche in Google Scholar

Magariños, A.M., Verdugo, J.M., and McEwen, B.S. (1997). Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. USA 94, 14002–14008.10.1073/pnas.94.25.14002Suche in Google Scholar

Magariños, A.M., Deslandes, A., and McEwen, B.S. (1999). Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur. J. Pharmacol. 371, 113–122.10.1016/S0014-2999(99)00163-6Suche in Google Scholar

Magariños, A.M., Li, C.J., Gal Toth, J., Bath, K.G., Jing, D., Lee, F.S., and McEwen, B.S. (2011). Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus 21, 253–264.10.1002/hipo.20744Suche in Google Scholar PubMed PubMed Central

Maggio, N. and Segal, M. (2009). Differential modulation of long-term depression by acute stress in the rat dorsal and ventral hippocampus. J. Neurosci. 29, 8633–8638.10.1523/JNEUROSCI.1901-09.2009Suche in Google Scholar PubMed PubMed Central

Maggio, N. and Segal, M. (2011). Persistent changes in ability to express long-term potentiation/depression in the rat hippocampus after juvenile/adult stress. Biol Psychiatry 69, 748–753.10.1016/j.biopsych.2010.11.026Suche in Google Scholar PubMed

Makena, N., Bugarith, K., and Russell, V.A. (2012). Maternal separation enhances object location memory and prevents exercise-induced MAPK/ERK signalling in adult Sprague-Dawley rats. Metab. Brain Dis. 27, 377–385.10.1007/s11011-012-9298-6Suche in Google Scholar PubMed PubMed Central

Maras, P.M. and Baram, T.Z. (2012). Sculpting the hippocampus from within: Stress, spines, and CRH. Trends Neurosci. 35, 315–324.10.1016/j.tins.2012.01.005Suche in Google Scholar PubMed PubMed Central

Maras, P.M., Molet, J., Chen, Y., Rice, C., Ji, S.G., Solodkin, A., and Baram, T.Z. (2014). Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress. Mol. Psychiatry 19, 811–822.10.1038/mp.2014.12Suche in Google Scholar PubMed PubMed Central

Marazziti, D., Consoli, G., Picchetti, M., Carlini, M., and Faravelli, L. (2010). Cognitive impairment in major depression. Eur. J. Pharmacol. 626, 83–86.10.1016/j.ejphar.2009.08.046Suche in Google Scholar

Marcuzzo, S., Dall’oglio, A., Ribeiro, M.F., Achaval, M., and Rasia-Filho, A.A. (2007). Dendritic spines in the posterodorsal medial amygdala after restraint stress and ageing in rats. Neurosci Lett. 424, 16–21.10.1016/j.neulet.2007.07.019Suche in Google Scholar

Mark, G.P., Rada, P.V., and Shors, T.J. (1996). Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala. Neuroscience 74, 767–774.10.1016/0306-4522(96)00211-4Suche in Google Scholar

Martisova, E., Solas, M., Horrillo, I., Ortega, J.E., Meana, J.J., Tordera, R.M., and Ramírez, M.J. (2012). Long lasting effects of early-life stress on glutamatergic/GABAergic circuitry in the rat hippocampus. Neuropharmacology 62, 1944–1953.10.1016/j.neuropharm.2011.12.019Suche in Google Scholar

McCall, T., Weil, Z.M., Nacher, J., Bloss, E.B., El Maarouf, A., Rutishauser, U., and McEwen, B.S. (2013). Depletion of polysialic acid from neural cell adhesion molecule (PSA-NCAM) increases CA3 dendritic arborization and increases vulnerability to excitotoxicity. Exp. Neurol. 241, 5–12.10.1016/j.expneurol.2012.11.028Suche in Google Scholar

McCormick, C.M., Nixon, F., Thomas, C., Lowie, B., and Dyck, J. (2010). Hippocampal cell proliferation and spatial memory performance after social instability stress in adolescence in female rats. Behav. Brain Res. 208, 23–29.10.1016/j.bbr.2009.11.003Suche in Google Scholar

McCormick, C.M., Thomas, C.M., Sheridan, C.S., Nixon, F., Flynn, J.A., and Mathews, I.Z., (2012). Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 22, 1300–1312.10.1002/hipo.20966Suche in Google Scholar

McEwen, B.S. (2003). Mood disorders and allostatic load. Biol. Psychiatry 54, 200–207.10.1016/S0006-3223(03)00177-XSuche in Google Scholar

McEwen, B.S. (2004). Protection and damage from acute and chronic stress: Allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann. NY Acad. Sci. 1032, 1–7.10.1196/annals.1314.001Suche in Google Scholar PubMed

McEwen, B.S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol. Rev. 87, 873–904.10.1152/physrev.00041.2006Suche in Google Scholar PubMed

McGuire, J., Herman, J.P., Horn, P.S., Sallee, F.R., and Sah, R. (2010). Enhanced fear recall and emotional arousal in rats recovering from chronic variable stress. Physiol. Behav. 101, 474–482.10.1016/j.physbeh.2010.07.013Suche in Google Scholar

McKittrick, C.R., Magarinos, A.M., Blanchard, D.C., Blanchard, R.J., McEwen, B.S., and Sakai, R.R. (2000). Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36, 85–94.10.1002/(SICI)1098-2396(200005)36:2<85::AID-SYN1>3.0.CO;2-YSuche in Google Scholar

Meaney, M.J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J.R., and Plotsky, P.M., (1996). Early environmental regulation of forebrain glucocorticoid receptor gene expression: Implications for adrenocortical responses to stress. Dev. Neurosci. 18, 49–72.10.1159/000111395Suche in Google Scholar

Menard, J.L., Champagne, D.L., and Meaney, M.J. (2004). Variations of maternal care differentially influence ‘fear’ reactivity and regional patterns of cFos immunoreactivity in response to the shock-probe burying test. Neuroscience 129, 297–308.10.1016/j.neuroscience.2004.08.009Suche in Google Scholar

Ming, G.L. and Song, H. (2005). Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28, 223–250.10.1146/annurev.neuro.28.051804.101459Suche in Google Scholar

Mineur, Y.S., Obayemi, A., Wigestrand, M.B., Fote, G.M., Calarco, C.A., Li, A.M., and Picciotto, M.R. (2013). Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc. Natl. Acad. Sci. USA 110, 3573–3578.10.1073/pnas.1219731110Suche in Google Scholar

Miura, H., Ando, Y., Noda, Y., Isobe, K., and Ozaki, N. (2011). Long-lasting effects of inescapable-predator stress on brain tryptophan metabolism and the behavior of juvenile mice. Stress 14, 262–272.10.3109/10253890.2010.541539Suche in Google Scholar

Mizoguchi, K., Kunishita, T., Chui, D.H., and Tabira, T. (1992). Stress induces neuronal death in the hippocampus of castrated rats. Neurosci. Lett. 138, 157–160.10.1016/0304-3940(92)90495-SSuche in Google Scholar

Mizoguchi, K., Shoji, H., Ikeda, R., Tanaka, Y., and Tabira, T. (2008). Persistent depressive state after chronic stress in rats is accompanied by HPA axis dysregulation and reduced prefrontal dopaminergic neurotransmission. Pharmacol. Biochem. Behav. 91, 170–175.10.1016/j.pbb.2008.07.002Suche in Google Scholar

Monroy, E., Hernández-Torres, E., and Flores, G. (2010). Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J. Chem. Neuroanat. 40, 93–101.10.1016/j.jchemneu.2010.05.005Suche in Google Scholar

Morilak, D.A., Barrera, G., Echevarria, D.J., Garcia, A.S., Hernandez, A., Ma, S., and Petre, C.O. (2005). Role of brain norepinephrine in the behavioral response to stress. Prog. Neuropsychopharmacol. Biol. Psychiatry 29, 1214–1224.Suche in Google Scholar

Mucha, M., Skrzypiec, A.E., Schiavon, E., Attwood, B.K., Kucerova, E., and Pawlak, R. (2011). Lipocalin-2 controls neuronal excitability and anxiety by regulating dendritic spine formation and maturation. Proc. Natl. Acad. Sci. USA 108, 18436–18441.10.1073/pnas.1107936108Suche in Google Scholar PubMed PubMed Central

Nair, A., Vadodaria, K.C., Banerjee, S.B., Benekareddy, M., Dias, B.G., Duman, R.S., and Vaidya, V.A. (2007). Stressor-specific regulation of distinct brain-derived neurotrophic factor transcripts and cyclic AMP response element-binding protein expression in the postnatal and adult rat hippocampus. Neuropsychopharmacology 32, 1504–1519.10.1038/sj.npp.1301276Suche in Google Scholar PubMed

Nijholt, I., Farchi, N., Kye, M., Sklan, E.H., Shoham, S., Verbeure, B., Owen, D., Hochner, B., Spiess, J., Soreq, H., et al. (2004). Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation. Mol. Psychiatry 9, 174–183.10.1038/sj.mp.4001446Suche in Google Scholar PubMed

O’Connor, R.M., Pusceddu, M.M., Dinan, T.G., and Cryan, J.F. (2013). Impact of early-life stress, on group III mGlu receptor levels in the rat hippocampus: Effects of ketamine, electroconvulsive shock therapy and fluoxetine treatment. Neuropharmacology 66, 236–241.10.1016/j.neuropharm.2012.05.006Suche in Google Scholar PubMed

Oitzl, M.S. and de Kloet, E.R. (1992). Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106, 62–71.10.1037/0735-7044.106.1.62Suche in Google Scholar

Oitzl, M.S., Fluttert, M., and de Kloet, E.R. (1994). The effect of corticosterone on reactivity to spatial novelty is mediated by central mineralocorticosteroid receptors. Eur. J. Neurosci. 6, 1072–1079.10.1111/j.1460-9568.1994.tb00604.xSuche in Google Scholar PubMed

O’Leary, O.F., Felice, D., Galimberti, S., Savignac, H.M., Bravo, J.A., Crowley, T., El Yacoubi, M., Vaugeois, J.M., Gassmann, M., Bettler, B., et al. (2014). GABAB(1) receptor subunit isoforms differentially regulate stress resilience. Proc. Natl. Acad. Sci. USA 111, 15232–15237.10.1073/pnas.1404090111Suche in Google Scholar PubMed PubMed Central

Olff, M., Langeland, W., and Gersons, B.P. (2005). The psychobiology of PTSD: Coping with trauma. Psychoneuroendocrinology 30, 974–982.10.1016/j.psyneuen.2005.04.009Suche in Google Scholar PubMed

O’Malley, D., Dinan, T.G., and Cryan, J.F. (2011). Neonatal maternal separation in the rat impacts on the stress responsivity of central corticotropin-releasing factor receptors in adulthood. Psychopharmacology (Berl). 214, 221–229.10.1007/s00213-010-1885-9Suche in Google Scholar PubMed

Oomen, C.A., Mayer, J.L., de Kloet, E.R., Joëls, M., and Lucassen, P.J. (2007). Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur. J. Neurosci. 26, 3395–3401.10.1111/j.1460-9568.2007.05972.xSuche in Google Scholar PubMed

Oomen, C.A., Girardi, C.E., Cahyadi, R., Verbeek, E.C., Krugers, H., Joëls, M., and Lucassen, P.J. (2009). Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS One 4, e3675.10.1371/journal.pone.0003675Suche in Google Scholar

Oomen, C.A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F.N., Manders, E.M., Joëls, M., Lucassen, P.J., and 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, 6635–6645.10.1523/JNEUROSCI.0247-10.2010Suche in Google Scholar

Oomen, C.A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F.N., Manders, E.M., Joëls M, Krugers, H., and Lucassen, P.J. (2011). Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats. Psychopharmacology (Berl). 214, 249–260.10.1007/s00213-010-1922-8Suche in Google Scholar

Oztan, Z., Aydin, C., and Isgor, C. (2011). Stressful environmental and social stimulation in adolescence causes antidepressant-like effects associated with epigenetic induction of the hippocampal BDNF and mossy fibre sprouting in the novelty-seeking phenotype. Neurosci. Lett. 501, 107–111.10.1016/j.neulet.2011.06.058Suche in Google Scholar

Pacak, K., Palkovits, M., Kopin, I.J., and Goldstein, D.S. (1995). Stress-induced norepinephrine release in the hypothalamic paraventricular nucleus and pituitary-adrenocortical and sympathoadrenal activity: In vivo microdialysis studies. Front Neuroendocrinol. 16, 89–150.10.1006/frne.1995.1004Suche in Google Scholar

Pan, B, Castro-Lopes, J.M., and Coimbra, A. (1999). Central afferent pathways conveying nociceptive input to the hypothalamic paraventricular nucleus as revealed by a combination of retrograde labeling and c-fos activation. J. Comp. Neurol. 413, 129–145.10.1002/(SICI)1096-9861(19991011)413:1<129::AID-CNE9>3.0.CO;2-QSuche in Google Scholar

Parfitt, G.M., Barbosa, Â.K., Campos, R.C., Koth, A.P., and Barros, D.M. (2012). Moderate stress enhances memory persistence: Are adrenergic mechanisms involved? Behav. Neurosci. 126, 729–734.Suche in Google Scholar

Parihar, V.K., Hattiangady, B., Kuruba, R., Shuai, B., and Shetty, A.K. (2011). Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol. Psychiatry 16, 171–183.10.1038/mp.2009.130Suche in Google Scholar

Park, C.R., Zoladz, P.R., Conrad, C.D., Fleshner, M., and Diamond, D.M. (2008). Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. Learn Mem. 15, 271–280.10.1101/lm.721108Suche in Google Scholar

Pavlides, C. and McEwen, B.S. (1999). Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field. Brain Res 851, 204–214.10.1016/S0006-8993(99)02188-5Suche in Google Scholar

Pavlides, C., Ogawa, S., Kimura, A., and McEwen, B.S. (1996). Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices. Brain Res. 738, 229–235.10.1016/S0006-8993(96)00776-7Suche in Google Scholar

Pavlides, C., Nivón, L.G., and McEwen, B.S. (2002). Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12, 245–257.10.1002/hipo.1116Suche in Google Scholar

Pawlak, R., Rao, B.S., Melchor, J.P., Chattarji, S., McEwen, B., and Strickland, S. (2005). Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc. Natl. Acad. Sci. USA 102, 18201–18206.10.1073/pnas.0509232102Suche in Google Scholar

Pickering, C., Gustafsson, L., Cebere, A., Nylander, I., and Liljequist, S. (2006). Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res. 1099, 101–108.10.1016/j.brainres.2006.04.136Suche in Google Scholar

Piroli, G.G., Grillo, C.A., Reznikov, L.R., Adams, S., McEwen, B.S., Charron, M.J., and Reagan, L.P. (2007). Corticosterone impairs insulin-stimulated translocation of GLUT4 in the rat hippocampus. Neuroendocrinology 85, 71–80.10.1159/000101694Suche in Google Scholar

Pollak, D.D., Monje, F.J., Zuckerman, L., Denny, C.A., Drew, M.R., and Kandel, E.R. (2008). An animal model of a behavioral intervention for depression. Neuron 60, 149–161.10.1016/j.neuron.2008.07.041Suche in Google Scholar

Quirarte, G.L., Roozendaal, B., and McGaugh, J.L. (1997). Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. USA 94, 14048–14053.10.1073/pnas.94.25.14048Suche in Google Scholar

Radecki, D.T., Brown, L.M., Martinez, J., and Teyler, T.J. (2005). BDNF protects against stress-induced impairments in spatial learning and memory and LTP. Hippocampus 15, 246–253.10.1002/hipo.20048Suche in Google Scholar

Radley, J.J. and Sawchenko, P.E. (2011). A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J. Neurosci. 31, 9683–9695.10.1523/JNEUROSCI.6040-10.2011Suche in Google Scholar

Reagan, L.P. and McEwen, B.S. (1997). Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J. Chem. Neuroanat. 13, 149–167.10.1016/S0891-0618(97)00031-8Suche in Google Scholar

Reich, C.G., Iskander, A.N., and Weiss, M.S. (2013). Cannabinoid modulation of chronic mild stress-induced selective enhancement of trace fear conditioning in adolescent rats. J. Psychopharmacol. 27, 947–955.10.1177/0269881113499207Suche in Google Scholar PubMed PubMed Central

Reul, J.M. and de Kloet, E.R. (1985). Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology 117, 2505–2511.10.1210/endo-117-6-2505Suche in Google Scholar PubMed

Rey, M., Carlier, E., Talmi, M., and Soumireu-Mourat, B. (1994). Corticosterone effects on long-term potentiation in mouse hippocampal slices. Neuroendocrinology 60, 36–41.10.1159/000126717Suche in Google Scholar PubMed

Rice, C.J., Sandman, C.A., Lenjavi, M.R., and Baram, T.Z. (2008). A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 149, 4892–4900.10.1210/en.2008-0633Suche in Google Scholar PubMed PubMed Central

Richter-Levin, G. (2004). The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10, 31–39.10.1177/1073858403259955Suche in Google Scholar PubMed

Roceri, M., Hendriks, W., Racagni, G., Ellenbroek, B.A., and Riva, M.A. (2002). Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol. Psychiatry 7, 609–616.10.1038/sj.mp.4001036Suche in Google Scholar PubMed

Rodríguez Manzanares, P.A., Isoardi, N.A., Carrer, H.F., and Molina, V.A. (2005). Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J. Neurosci. 25, 8725–8734.10.1523/JNEUROSCI.2260-05.2005Suche in Google Scholar PubMed PubMed Central

Roozendaal, B., Griffith, Q.K., Buranday, J., De Quervain, D.J., and McGaugh, J.L. (2003). The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: Dependence on the basolateral amygdala. Proc. Natl. Acad. Sci. USA 100, 1328–1333.10.1073/pnas.0337480100Suche in Google Scholar PubMed PubMed Central

Roozendaal, B., McEwen, B.S., and Chattarji, S. (2009). Stress, memory and the amygdala. Nat. Rev. Neurosci. 10, 423–433.10.1038/nrn2651Suche in Google Scholar PubMed

Rosoklija, G., Toomayan, G., Ellis, S.P., Keilp, J., Mann, J.J., Latov, N., Hays, A.P., and Dwork, A.J. (2000). Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: Preliminary findings. Arch Gen Psychiatry 57, 349–356.10.1001/archpsyc.57.4.349Suche in Google Scholar PubMed

Roy, M. and Sapolsky, R.M. (2003). The exacerbation of hippocampal excitotoxicity by glucocorticoids is not mediated by apoptosis. Neuroendocrinology 77, 24–31.10.1159/000068337Suche in Google Scholar PubMed

Ryan, B.K., Vollmayr, B., Klyubin, I., Gass, P., and Rowan, M.J. (2010). Persistent inhibition of hippocampal long-term potentiation in vivo by learned helplessness stress. Hippocampus 20, 758–767.10.1002/hipo.20677Suche in Google Scholar

Rygula, R., Abumaria, N., Flügge, G., Fuchs, E., Rüther, E., and Havemann-Reinecke, U. (2005). Anhedonia and motivational deficits in rats: Impact of chronic social stress. Behav. Brain Res. 162, 127–134.10.1016/j.bbr.2005.03.009Suche in Google Scholar

Salehi, B., Cordero, M.I., and Sandi, C. (2010). Learning under stress: The inverted-U-shape function revisited. Learn Mem. 17, 522–530.10.1101/lm.1914110Suche in Google Scholar

Sandi, C. and Pinelo-Nava, M.T. (2007). Stress and memory: Behavioral effects and neurobiological mechanisms. Neural Plast. 2007, 78970.10.1155/2007/78970Suche in Google Scholar

Sandi, C., Loscertales, M., and Guaza, C. (1997). Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 9, 637–642.10.1111/j.1460-9568.1997.tb01412.xSuche in Google Scholar

Sapolsky, R.M. (1985). A mechanism for glucocorticoid toxicity in the hippocampus: Increased neuronal vulnerability to metabolic insults. J. Neurosci. 5, 1228–1232.10.1523/JNEUROSCI.05-05-01228.1985Suche in Google Scholar

Sapolsky, R.M. and Meaney, M.J. (1986). Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 396, 64–76.10.1016/0165-0173(86)90010-XSuche in Google Scholar

Sapolsky, R.M., Uno, H., Rebert, C.S., and Finch, C.E. (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J. Neurosci. 10, 2897–2902.10.1523/JNEUROSCI.10-09-02897.1990Suche in Google Scholar

Sapolsky, R.M., Romero, L.M., and Munck, A.U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55–89.Suche in Google Scholar

Schasfoort, E.M., De Bruin, L.A., and Korf, J. (1988). Mild stress stimulates rat hippocampal glucose utilization transiently via NMDA receptors, as assessed by lactography. Brain Res. 475, 58–63.10.1016/0006-8993(88)90198-9Suche in Google Scholar

Schloesser, R.J., Manji, H.K., and Martinowich, K. (2009). Suppression of adult neurogenesis leads to an increased hypothalamo-pituitary-adrenal axis response. Neuroreport 20, 553–557.10.1097/WNR.0b013e3283293e59Suche in Google Scholar PubMed PubMed Central

Schmidt, M.V. (2011). Animal models for depression and the mismatch hypothesis of disease. Psychoneuroendocrinology 36, 330–338.10.1016/j.psyneuen.2010.07.001Suche in Google Scholar

Schmidt, H.D. and Duman, R.S. (2007). The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav. Pharmacol. 18, 391–418.10.1097/FBP.0b013e3282ee2aa8Suche in Google Scholar

Schmidt, H.D. and Duman, R.S. (2010). Peripheral BDNF produces antidepressant-like effects in cellular and behavioral models. Neuropsychopharmacology 35, 2378–2391.10.1038/npp.2010.114Suche in Google Scholar

Schmidt, M.V., Enthoven, L., van der Mark, M., Levine, S., de Kloet, E.R., and Oitzl, M.S., 2003. The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. Int. J. Dev. Neurosci. 21, 125–132.10.1016/S0736-5748(03)00030-3Suche in Google Scholar

Schoenfeld, T.J. and Gould, E. (2012). Stress, stress hormones, and adult neurogenesis. Exp. Neurol. 233, 12–21.10.1016/j.expneurol.2011.01.008Suche in Google Scholar

Segev, A., Ramot, A., and Akirav, I. (2012). Stress hormones receptors in the amygdala mediate the effects of stress on the consolidation, but not the retrieval, of a non aversive spatial task. PLoS One 7, e29988.10.1371/journal.pone.0029988Suche in Google Scholar

Shalev, A.Y., Freedman, S., Peri, T., Brandes, D., Sahar, T., Orr, S.P., and Pitman, R.K. (1998). Prospective study of posttraumatic stress disorder and depression following trauma. Am. J. Psychiatry 155, 630–637.10.1176/ajp.155.5.630Suche in Google Scholar

Sheline, Y.I., Wang, P.W., Gado, M.H., Csernansky, J.G., and Vannier, M.W. (1996). Hippocampal atrophy in recurrent major depression. Proc. Natl. Acad. Sci. USA 93, 3908–3913.10.1073/pnas.93.9.3908Suche in Google Scholar

Shimizu, E., Hashimoto, K., Okamura, N., Koike, K., Komatsu, N., Kumakiri, C., Nakazato, M., Watanabe, H., Shinoda, N., Okada, S., et al. (2003). Alterations of serum levels of brain derived neurotrophic factor (BDNF) in depressed patients with or without antidepressants. Biol. Psychiatry 54, 70–75.10.1016/S0006-3223(03)00181-1Suche in Google Scholar

Shors, T. J. (2001). Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol. Learn. Mem. 75, 10–29.10.1006/nlme.1999.3956Suche in Google Scholar PubMed

Shors, T.J. (2006). Stressful experience and learning across the lifespan. Annu. Rev. Psychol. 57, 55–85.10.1146/annurev.psych.57.102904.190205Suche in Google Scholar

Shors, T.J., Seib, T.B., Levine, S., and Thompson, R.F. (1989). Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244, 224–226.10.1126/science.2704997Suche in Google Scholar

Shors, T.J., Weiss, C., and Thompson, R.F. (1992). Stress-induced facilitation of classical conditioning. Science 257, 537–539.10.1126/science.1636089Suche in Google Scholar

Shors, T.J., Chua, C., and Falduto, J. (2001). Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J. Neurosci. 21, 6292–6297.10.1523/JNEUROSCI.21-16-06292.2001Suche in Google Scholar

Smith, S.M. and Vale, W.W. (2006). The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin. Neurosci. 8, 383–395.10.31887/DCNS.2006.8.4/ssmithSuche in Google Scholar

Smith, D.W., Buller, K.M., and Day, T.A. (1995). Role of ventrolateral medulla catecholamine cells in hypothalamic neuroendocrine cell responses to systemic hypoxia. J. Neurosci. 15, 7979–7988.10.1523/JNEUROSCI.15-12-07979.1995Suche in Google Scholar

Smith, G.W., Aubry, J.M., Dellu, F., Contarino, A., Bilezikjian, L.M., Gold, L.H., Chen, R., Marchuk, Y., Hauser, C., Bentley, C.A., et al. (1998). Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20, 1093–1102.10.1016/S0896-6273(00)80491-2Suche in Google Scholar

Snyder, J.S., Soumier, A., Brewer, M., Pickel, J., and Cameron, H.A. (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behavior. Nature 476, 458–461.10.1038/nature10287Suche in Google Scholar PubMed PubMed Central

Soetanto, A., Wilson, R.S., Talbot, K., Un, A., Schneider, J.A., Sobiesk, M., Kelly, J., Leurgans, S., Bennett, D.A., and Arnold, S.E. (2010). Association of anxiety and depression with microtubule-associated protein 2- and synaptopodin-immunolabeled dendrite and spine densities in hippocampal CA3 of older humans. Arch. Gen. Psychiatry 67, 448–457.10.1001/archgenpsychiatry.2010.48Suche in Google Scholar PubMed PubMed Central

Son, H., Banasr, M., Choi, M., Chae, S.Y., Licznerski, P., Lee, B., Voleti, B., Li, N., Lepack, A., Fournier, N.M., et al. (2012). Neuritin produces antidepressant actions and blocks the neuronal and behavioral deficits caused by chronic stress. Proc. Natl. Acad. Sci. USA 109, 11378–11383.10.1073/pnas.1201191109Suche in Google Scholar PubMed PubMed Central

Song, L., Che, W., Min-Wei, W., Murakami, Y., and Matsumoto, K. (2006). Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol. Biochem. Behav. 83, 186–193.10.1016/j.pbb.2006.01.004Suche in Google Scholar

Sousa, N., Almeida, O.F., Holsboer, F., Paula-Barbosa, M.M., and Madeira, M.D. (1998). Maintenance of hippocampal cell numbers in young and aged rats submitted to chronic unpredictable stress. Comparison with the effects of corticosterone treatment. Stress 2, 237–249.10.3109/10253899809167288Suche in Google Scholar

Sousa, N., Lukoyanov, N.V., Madeira, M.D., Almeida, O.F., and Paula-Barbosa, M.M. (2000). Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97, 253–266.10.1016/S0306-4522(00)00050-6Suche in Google Scholar

Sousa, V.C., Vital, J., Costenla, A.R., Batalha, V.L., Sebastiao, A.M., Ribeiro, J.A., and Lopes, L.V. (2014). Maternal separation impairs long term-potentiation in CA1-CA3 synapses and hippocampal-dependent memory in old rats. Neurobiol. Aging 35, 1680–1685.10.1016/j.neurobiolaging.2014.01.024Suche in Google Scholar

Spyrka, J., Danielewicz, J., and Hess, G. (2011). Brief neck restraint stress enhances long-term potentiation and suppresses long-term depression in the dentate gyrus of the mouse. Brain Res. Bull. 85, 363–367.10.1016/j.brainresbull.2011.05.008Suche in Google Scholar

Stein-Behrens, B., Mattson, M.P., Chang, I., Yeh, M., and Sapolsky, R. (1994). Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. J. Neurosci. 14, 5373–5380.10.1523/JNEUROSCI.14-09-05373.1994Suche in Google Scholar

Sterlemann, V., Rammes, G., Wolf, M., Liebl, C., Ganea, K., Müller, M.B., and Schmidt, M.V. (2010). Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 20, 540–549.Suche in Google Scholar

Stockmeier, C.A., Mahajan, G.J., Konick, L.C., Overholser, J.C., Jurjus, G.J., Meltzer, H.Y., Uylings, H.B., Friedman, L., and Rajkowska, G. (2004). Cellular changes in the postmortem hippocampus in major depression. Biol. Psychiatry 56, 640–650.10.1016/j.biopsych.2004.08.022Suche in Google Scholar

Stokes, P.E. (1995). The potential role of excessive cortisol induced by HPA hyperfunction in the pathogenesis of depression. Eur. Neuropsychopharmacol. 5, (Suppl), 77–82.10.1016/0924-977X(95)00039-RSuche in Google Scholar

Strekalova, T., Spanagel, R., Bartsch, D., Henn, F.A., and Gass, P. (2004). Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29, 2007–2017.10.1038/sj.npp.1300532Suche in Google Scholar

Sunanda, Meti, B.L., and Raju, T.R. (1997). Entorhinal cortex lesioning protects hippocampal CA3 neurons from stress-induced damage. Brain Res. 770, 302–306.10.1016/S0006-8993(97)00888-3Suche in Google Scholar

Suo, L., Zhao, L., Si, J., Liu, J., Zhu, W., Chai, B., Zhang, Y., Feng, J., Ding, Z., Luo, Y., Shi, H., Shi, J., Lu, L. (2013). Predictable chronic mild stress in adolescence increases resilience in adulthood. Neuropsychopharmacology 38: 1387–1400.Suche in Google Scholar

Suri, D., Bhattacharya, A., and Vaidya, V.A. (2014). Early stress evokes temporally distinct consequences on the hippocampal transcriptome, anxiety and cognitive behaviour. Int. J. Neuropsychopharmacol. 12, 1–13.10.1017/S1461145713001004Suche in Google Scholar PubMed

Suri, D., Veenit, V., Sarkar, A., Thiagarajan, D., Kumar, A., Nestler, E.J., Galande, S., and Vaidya, V.A. (2013). Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition. Biol. Psychiatry 73, 658–666.10.1016/j.biopsych.2012.10.023Suche in Google Scholar PubMed PubMed Central

Swinny, J.D., O’Farrell, E., Bingham, B.C., Piel, D.A., Valentino, R.J., and Beck, S.G. (2010). Neonatal rearing conditions distinctly shape locus coeruleus neuronal activity, dendritic arborization, and sensitivity to corticotrophin-releasing factor. Int. J. Neuropsychopharmacol. 13, 515–525.10.1017/S146114570999037XSuche in Google Scholar PubMed PubMed Central

Takahashi, T., Kimoto, T., Tanabe, N., Hattori, T.A., Yasumatsu, N., and Kawato, S. (2002). Corticosterone acutely prolonged N-methyl-d-aspartate receptor-mediated Ca²⁺ elevation in cultured rat hippocampal neurons. J. Neurochem. 83, 1441–1451.10.1046/j.1471-4159.2002.01251.xSuche in Google Scholar PubMed

Takeda, A., Ando, M., Kanno, S., and Oku, N. (2009). Unique response of zinc in the hippocampus to behavioral stress and attenuation of subsequent mossy fiber long-term potentiation. Neurotoxicology 30, 712–717.10.1016/j.neuro.2009.05.009Suche in Google Scholar PubMed

Tanapat, P., Hastings, N.B., Rydel, T.A., Galea, L.A., and Gould, E. (2001). Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol. 437, 496–504.10.1002/cne.1297Suche in Google Scholar PubMed

Tang, A.C., Reeb, B.C., Romeo, R.D., and McEwen, B.S. (2003). Modification of social memory, hypothalamic-pituitary-adrenal axis, and brain asymmetry by neonatal novelty exposure. J. Neurosci. 23, 8254–8260.10.1523/JNEUROSCI.23-23-08254.2003Suche in Google Scholar

Tang, A.C., Akers, K.G., Reeb, B.C., Romeo, R.D., and McEwen, B.S. (2006). Programming social, cognitive, and neuroendocrine development by early exposure to novelty. Proc. Natl. Acad. Sci. USA 103, 15716–15721.10.1073/pnas.0607374103Suche in Google Scholar PubMed PubMed Central

Teicher, M.H., Anderson, C.M., and Polcari, A. (2012). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc. Natl. Acad. Sci. USA 109, 563–572.10.1073/pnas.1115396109Suche in Google Scholar PubMed PubMed Central

Thomas, R.M., Hotsenpiller, G., and Peterson, D.A. (2007). Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J. Neurosci. 27, 2734–2743.10.1523/JNEUROSCI.3849-06.2007Suche in Google Scholar PubMed PubMed Central

Thorsell, A., Michalkiewicz, M., Dumont, Y., Quirion, R., Caberlotto, L., Rimondini, R., Mathé, A.A., and Heilig, M. (2000). Behavioral insensitivity to restraint stress, absent fear suppression of behavior and impaired spatial learning in transgenic rats with hippocampal neuropeptide Y overexpression. Proc. Natl. Acad. Sci. USA 97, 12852–12857.10.1073/pnas.220232997Suche in Google Scholar

Timpl, P., Spanagel, R., Sillaber, I., Kresse, A., Reul, J.M., Stalla, G.K., Blanquet, V., Steckler, T., Holsboer, F., and Wurst, W. (1998). Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat. Genet. 19, 162–166.10.1038/520Suche in Google Scholar

Tyrka, A.R., Price, L.H., Kao, H.T., Porton, B., Marsella, S.A., and Carpenter, L.L. (2010). Childhood maltreatment and telomere shortening: Preliminary support for an effect of early stress on cellular aging. Biol. Psychiatry 67, 531–534.10.1016/j.biopsych.2009.08.014Suche in Google Scholar

Uher, R. (2009). The role of genetic variation in the causation of mental illness: An evolution-informed framework. Mol. Psychiatry 14, 1072–1082.10.1038/mp.2009.85Suche in Google Scholar

Uno, H., Tarara, R., Else, J.G., Suleman, M.A., and Sapolsky, R.M. (1989). Hippocampal damage associated with prolonged and fatal stress in primates. J. Neurosci. 9, 1705–1711.10.1523/JNEUROSCI.09-05-01705.1989Suche in Google Scholar

Uysal, N., Sisman, A.R., Dayi, A., Ozbal, S., Cetin, F., Baykara, B., Aksu, I., Tas, A., Cavus, S.A., Gonenc-Arda, S., et al. (2012). Acute footshock-stress increases spatial learning-memory and correlates to increased hippocampal BDNF and VEGF and cell numbers in adolescent male and female rats. Neurosci. Lett. 514, 141–146.10.1016/j.neulet.2012.02.049Suche in Google Scholar

Vander Weele, C.M., Saenz, C., Yao, J., Correia, S.S., and Goosens, K.A. (2013). Restoration of hippocampal growth hormone reverses stress-induced hippocampal impairment. Front. Behav. Neurosci. 7, 66.Suche in Google Scholar

van Hasselt, F.N., Boudewijns, Z.S., van der Knaap, N.J., Krugers, H.J., and Joëls, M. (2012). Maternal care received by individual pups correlates with adult CA1 dendritic morphology and synaptic plasticity in a sex-dependent manner. J. Neuroendocrinol. 24, 331–340.10.1111/j.1365-2826.2011.02233.xSuche in Google Scholar

van Oers, H.J., de Kloet, E.R., and Levine, S. (1998). Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Brain Res. Dev. Brain Res. 111, 245–252.10.1016/S0165-3806(98)00143-6Suche in Google Scholar

van Stegeren, A.H., Wolf, O.T., Everaerd, W., Scheltens, P., Barkhof, F., and Rombouts, S.A. (2007). Endogenous cortisol level interacts with noradrenergic activation in the human amygdala. Neurobiol. Learn Mem. 87, 57–66.10.1016/j.nlm.2006.05.008Suche in Google Scholar PubMed

van Stegeren, A.H., Roozendaal, B., Kindt, M., Wolf, O.T., and Joëls, M. (2010). Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding. Neurobiol. Learn. Mem. 93, 56–65.10.1016/j.nlm.2009.08.004Suche in Google Scholar PubMed

Veena, J., Srikumar, B.N., Raju, T.R., and Shankaranarayana Rao, B.S. (2009). Exposure to enriched environment restores the survival and differentiation of new born cells in the hippocampus and ameliorates depressive symptoms in chronically stressed rats. Neurosci. Lett. 455, 178–182.10.1016/j.neulet.2009.03.059Suche in Google Scholar

Vidal, J., Bie, Jd., Granneman, R.A., Wallinga, A.E., Koolhaas, J.M., and Buwalda, B. (2007). Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiol. Behav. 92, 824–830.10.1016/j.physbeh.2007.06.004Suche in Google Scholar

Vollmann-Honsdorf, G.K., Flügge, G., and Fuchs, E. (1997). Chronic psychosocial stress does not affect the number of pyramidal neurons in tree shrew hippocampus. Neurosci. Lett. 233, 121–124.10.1016/S0304-3940(97)00647-2Suche in Google Scholar

Vyas, A., Mitra, R., Shankaranarayana Rao, B.S., and Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 22, 6810–6818.10.1523/JNEUROSCI.22-15-06810.2002Suche in Google Scholar

Wagner, K.V., Hartmann, J., Mangold, K., Wang, X.D., Labermaier, C., Liebl, C., Wolf, M., Gassen, N.C., Holsboer, F., Rein, T., et al. (2013). Homer1 mediates acute stress-induced cognitive deficits in the dorsal hippocampus. J. Neurosci. 33, 3857–3864.10.1523/JNEUROSCI.4333-12.2013Suche in Google Scholar

Wang, H. and Gondré-Lewis, M.C., 2013. Prenatal nicotine and maternal deprivation stress de-regulate the development of CA1, CA3, and dentate gyrus neurons in hippocampus of infant rats. PLoS One 8, e65517.10.1371/journal.pone.0065517Suche in Google Scholar

Wang, X.D., Chen, Y., Wolf, M., Wagner, K.V., Liebl, C., Scharf, S.H., Harbich, D., Mayer, B., Wurst, W., Holsboer, F., et al. (2011a). Forebrain CRHR1 deficiency attenuates chronic stress-induced cognitive deficits and dendritic remodeling. Neurobiol. Dis. 42, 300–310.10.1016/j.nbd.2011.01.020Suche in Google Scholar

Wang, X.D., Rammes, G., Kraev, I., Wolf, M., Liebl, C., Scharf, S.H., Rice, C.J., Wurst, W., Holsboer, F., Deussing, J.M., et al. (2011b). Forebrain CRF modulates early-life stress-programmed cognitive deficits. J. Neurosci. 31, 13625–13634.10.1523/JNEUROSCI.2259-11.2011Suche in Google Scholar

Watanabe, Y., Gould, E., and McEwen, B.S. (1992). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588, 341–345.10.1016/0006-8993(92)91597-8Suche in Google Scholar

Weaver, I.C., Grant, R.J., and Meaney, M.J. (2002). Maternal behavior regulates long-term hippocampal expression of BAX and apoptosis in the offspring. J. Neurochem. 82, 998–1002.10.1046/j.1471-4159.2002.01054.xSuche in Google Scholar PubMed

Weaver, I.C., Cervoni, N., Champagne, F.A., D’Alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M., and Meaney, M.J. (2004). Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847–854.10.1038/nn1276Suche in Google Scholar PubMed

Weaver, I.C., Meaney, M.J., and Szyf, M. (2006). Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl. Acad. Sci. USA 103, 3480–3485.10.1073/pnas.0507526103Suche in Google Scholar PubMed PubMed Central

Wood, G.E., Norris, E.H., Waters, E., Stoldt. J.T., and McEwen, B.S. (2008). Chronic immobilization stress alters aspects of emotionality and associative learning in the rat. Behav. Neurosci. 122, 282–292.10.1037/0735-7044.122.2.282Suche in Google Scholar PubMed

Wong, T.P., Howland, J.G., Robillard, J.M., Ge, Y., Yu, W., Titterness, A.K., Brebner, K., Liu, L., Weinberg, J., Christie, B.R., et al. (2007). Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment. Proc. Natl. Acad. Sci. USA 104, 11471–11476.10.1073/pnas.0702308104Suche in Google Scholar PubMed PubMed Central

Xu, L., Anwyl, R., and Rowan, M.J. (1997). Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387, 497–500.10.1038/387497a0Suche in Google Scholar PubMed

Yang, C.H., Huang, C.C., and Hsu, K.S. (2004). Behavioral stress modifies hippocampal synaptic plasticity through corticosterone-induced sustained extracellular signal-regulated kinase/mitogen-activated protein kinase activation. J. Neurosci. 24, 11029–11034.10.1523/JNEUROSCI.3968-04.2004Suche in Google Scholar PubMed PubMed Central

Yoshiike, Y., Yamashita, S., Mizoroki, T., Maeda, S., Murayama, M., Kimura, T., Sahara, N., Soeda, Y., and Takashima, A. (2012). Adaptive responses to alloxan-induced mild oxidative stress ameliorate certain tauopathy phenotypes. Aging Cell 11, 51–62.10.1111/j.1474-9726.2011.00756.xSuche in Google Scholar PubMed

Young, E.A., Haskett, R.F., Murphy-Weinberg, V., Watson, S.J., and Akil, H. (1991). Loss of glucocorticoid fast feedback in depression. Arch. Gen. Psychiatry 48, 693–699.10.1001/archpsyc.1991.01810320017003Suche in Google Scholar PubMed

Zhou, Q.G., Hu, Y., Wu, D.L., Zhu, L.J., Chen, C., Jin, X., Luo, C.X., Wu, H.Y., Zhang, J., and Zhu, D.Y. (2011). Hippocampal telomerase is involved in the modulation of depressive behaviors. J. Neurosci. 31, 12258–12269.10.1523/JNEUROSCI.0805-11.2011Suche in Google Scholar PubMed PubMed Central