The effects of chronic restraint on the morphology of ventral CA1 neurons in female Long Evans rats

References

• Akirav I, Levin GR. (2002). Mechanisms of amygdala modulation of hippocampal plasticity. J Neurosci 22:9912–21
   PubMed Web of Science ®Google Scholar
• Argumedo SG, Martínez-Ávila MA, Peraza VA, Zavala Gonzáles MA, Rojas GL, Mejía-Barragán GM. (2007). Efecto protector del pirofosfato de tiamina en el hipocampo de ratas expuestas a estrés por inmovilización forzada. Vet Mex 38:429–38
   Google Scholar
• Bisagno V, Bowman RE, Luine VN. (2003). Functional aspects of estrogen neuroprotection. Endocrine 21:33–41
   PubMed Web of Science ®Google Scholar
• Bowman RE, Beck KD, Luine VN. (2003). Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm Behav 43:48–59
   PubMed Web of Science ®Google Scholar
• Bowman RE, Zrull MC, Luine VN. (2001). Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res 904:279–89
   PubMed Web of Science ®Google Scholar
• Christian KM, Miracle AD, Wellman CL, Nakazawa K. (2011). Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 174:26–36
   PubMed Web of Science ®Google Scholar
• Conrad CD, Galea LA, Kuroda Y, McEwen BS. (1996). Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 110:1321–34
   PubMed Web of Science ®Google Scholar
• Conrad CD, McLaughlin KJ, Harman JS, Foltz C, Wieczorek L, Lightner E, Wright RL. (2007). Chronic glucocorticoids increase hippocampal vulnerabilitily to neurotoxicity under conditions that produce CA3 dendritic retraction but fail to impair spatial recognition memory. J Neurosci 27(31):8278–85
   PubMed Web of Science ®Google Scholar
• Conrad CD. (2006). What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus? Behav Cogn Neurosci Rev 5(1):41–60
   PubMedGoogle Scholar
• Cook SC, Wellman CL. (2004). Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60:236–48
   PubMed Web of Science ®Google Scholar
• Eiland L, Ramroop J, Hill MN, Manley J, McEwen BS. (2012). Chronic juvenile stress produces coritoclimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 37:39–47
   PubMed Web of Science ®Google Scholar
• Epp JR, Scott NA, Galea LAM. (2011). Strain differences in neurogenesis and activation of new neurons in the dentate gyrus in response to spatial learning. Neuroscience 172:342–54
   PubMed Web of Science ®Google Scholar
• Fanselow MS, Dong H-W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65(1):7–19
   PubMed Web of Science ®Google Scholar
• Flores G, Alquicer G, Silva-Gómez AB, Rivera G, Quirion R, Srivastava K. (2005). Alterations in dendritic morphology of prefrontal cortical and nucleus acumbens neurons in adult rats after neonatal excitotoxic lesions of the ventral hippocampus. Neuroscience 133(2):463–70
   PubMed Web of Science ®Google Scholar
• Galea LA, McEwen BS, Tanapat P, Deak T, Spence RL, Dhabhar FS. (1997). Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81:689–97
   PubMed Web of Science ®Google Scholar
• Garrett JE, Wellman CL. (2009). Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 162:195–207
   PubMed Web of Science ®Google Scholar
• Gerrits M, Westenbroek C, Fokkema DS, Jongsma ME, Den Boer JA, Ter Horst GJ. (2003). Increased stress vulnerability after a prefrontal cortex lesion in female rats. Brain Res Bull 61:627–35
   PubMed Web of Science ®Google Scholar
• Ghadrdoost B, Vafaei AA, Rashidy-Pour A, Hajisoltani R, Bandegi AR, Motamedi F, Haghighi S, et al. (2011). Protective effects of saffron extract and its active constituent crocin against oxidative stress and spatial learning and memory deficits induced by chronic stress in rats. Eur J Pharmacol 667(1–3):222–9
   PubMed Web of Science ®Google Scholar
• Gibb R, Kolb B. (1998). A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 79:1–4
   PubMed Web of Science ®Google Scholar
• Gould E, Woolley CS, Frankfurt M, McEwen BS. (1990). Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10(4):1286–91
   PubMed Web of Science ®Google Scholar
• Hajszan T, Maclusky NJ, Leranth C. (2004). Dehydroepiandrosterone increases hippocampal spine synapse density in ovariectomized female rats. Endocrinology 145(3):1042–5
   PubMed Web of Science ®Google Scholar
• Haynes LE, Barber D, Mitchell IJ. (2004). Chronic antidepressant medication attenuates dexamethasone-induced neuronal death and sublethal neuronal damage in the hippocampus and striatum. Brain Res 1026:157–67
   PubMed Web of Science ®Google Scholar
• Hoffman GE, Merchenthaler I, Zup SL. (2006). Neuroprotection by ovarian hormones in animal models of neurological disease. Endocrine 29(2):217–31
   PubMed Web of Science ®Google Scholar
• Horner CH, Arbuthnott E. (1991). Methods of estimation of spine density – are spines evenly distributed throughout the dendritic field? J Anat 177:179–84
   PubMed Web of Science ®Google Scholar
• Horner CH, O’Regan M, Arbuthnott E. (1991). Neural plasticity of the hippocampal (CA1) pyramidal cell-quantitative changes in spine density following handling and injection for drug testing. JAnat 174:229–38
   Google Scholar
• Hosseini-sharifabad M, Hadinedoushan H. (2007). Prenatal stress induces learning deficits and is associated with a decrease in granules and CA3 cell dendritic tree size in rat hippocampus. Anat Sci Int 82:211–17
   PubMed Web of Science ®Google Scholar
• Hutchinson KM, McLaughlin KJ, Wright RL, Ortiz JB, Anouti DP, Mika A, Diamond DM, Conrad CD. (2012). Environmental enrichment protects against effects of chronic stress on cognitive and morphological measures of hippocampal integrity. Neurobiol Learn Mem 97:250–60
   PubMed Web of Science ®Google Scholar
• Juárez I, Gratton A, Flores G. (2008). Ontogeny of altered dendritic morphology in the rat prefrontal cortex, hippocampus, and nucleus accumbens following cesarean delivery and birth anoxia. J Comp Neurol 507:1734–47
   PubMed Web of Science ®Google Scholar
• Kim JJ, Diamond DM. (2002). The stressed hippocampus, synaptic plasticity and lost memory. Nature 3:453–62
   Web of Science ®Google Scholar
• Krugers HJ, Goltstein PM, van der Linden S, Joëls M. (2006). Blockade of glucocorticoid receptors rapidly restores hippocampal CA1 synaptic plasticity after exposure to chronic stress. Eur J Neurosci 23:3051–5
   PubMed Web of Science ®Google Scholar
• Lambert KG, Buckelew SK, Staffiso-Sandoz G, Gaffga S, Carpenter W, Fisher J, Kinsley CH. (1998). Activity-stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats. Physiol Behav 65(1):43–9
   PubMed Web of Science ®Google Scholar
• Li C, Brake WG, Romeo RD, Dunlop JC, Gordon M, Buzescu R, Magariños AM, et al. (2004). Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc Natl Acad Sci USA 101(7):2185–90
   PubMed Web of Science ®Google Scholar
• Luine V, Villegas M, Martinez C, McEwen BS. (1994). Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167–70
   PubMed Web of Science ®Google Scholar
• Luine V. (2002). Sex differences in chronic stress effects on memory in rats. Stress 5:205–16
   PubMed Web of Science ®Google Scholar
• Magariños AM, García-Verduga JM, McEwen BS. (1997). Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci USA 94:14002–8
   PubMed Web of Science ®Google Scholar
• Magariños AM, McEwen BS, Flügge G, Fuchs E. (1996). Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16(10):3534–40
   PubMed Web of Science ®Google Scholar
• Martínez-Téllez RI, Hernández-Torres E, Gamboa C, Flores G. (2009). Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 63:794–804
   PubMed Web of Science ®Google Scholar
• McKittrick CR, Magariños AM, Blanchard DC, Blanchard RJ, McEwen BS, Sakaf RR. (2000). Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36:85–94
   PubMed Web of Science ®Google Scholar
• McLaughlin KJ, Baran SE, Wright RL, Conrad CD. (2005). Chronic stress enhanced spatial memory in ovariectomized female rats despite CA3 dendritic retraction: possible involvement of CA1 neurons. Neuroscience 135:1045–54
   PubMed Web of Science ®Google Scholar
• McLaughlin KJ, Gomez J, Baran SE, Conrad CD. (2007). The effects of chronic stress on hipocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 1161:56–64
   PubMed Web of Science ®Google Scholar
• Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S. (2005). Stress duration modulates the spatiotemporal patterns of spine formation in the basilar amygdale. Proc Natl Acad Sci USA 102:9371–6
   PubMed Web of Science ®Google Scholar
• Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Chui DH, Tabira T. (2000). Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 20:1568–74
   PubMed Web of Science ®Google Scholar
• Morales-Medina JC, Sanchez F, Flores G, Dumont Y, Quirion R. (2009). Morphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J Chem Neuroanat 38:266–72
   PubMed Web of Science ®Google Scholar
• Morris R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47–60
   PubMed Web of Science ®Google Scholar
• Muñoz-Cueto JA, García-Segura LM, Ruiz-Marcos A. (1990). Developmental sex differences and effect of ovariectomy on the numbrer of cortical piramidal cell dendritic spines. Brain Res 515:64–8
   PubMed Web of Science ®Google Scholar
• Murakami G, Tsurugizawa T, Hatanaka Y, Komatsuzaki Y, Tanabe N, Mukai H, Hojo Y, et al. (2006). Comparison between basal and apical dendritic spines in estrogen-induced rapid spinogenesis of CA1 principal neurons in the adult hippocampus. Biochem Biophys Res Commun 351(2):553–8
   PubMed Web of Science ®Google Scholar
• Pare WP. (1990). Technique and strain comparisons in stress ulcer. Ann NY Acad Sci 597:223–30
   PubMed Web of Science ®Google Scholar
• Paxinos G, Watson C. (1998). The rat brain in stereotaxic coordinates. 4th ed. New York: Academic Press
   Google Scholar
• Perez-Cruz C, Muller-Keuker JIH, Heilbronner U, Fuchs E, Flugge G. (2007). Morphology of pyramidal neurons in the rat prefrontal cortex: lateralized dendritic remodeling by chronic stress. Neural Plasticity 2007:1–14
   Google Scholar
• Prendergast BJ, Onishi KG, Zucker I. (2014). Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci Biobehav Rev 40:1–5
   PubMed Web of Science ®Google Scholar
• Prusky GT, Harker KT, Douglas RM, Whishaw IQ. (2002). Variation in visual acuity within pigmented, and between pigmented and albino rat strains. Behav Brain Res 136:339–48
   PubMed Web of Science ®Google Scholar
• Radley JJ, Rocher AB, Miller M, Janssen WGM, Liston C, Hof PR, McEwen BS, Morrison HJ. (2006). Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cerebral Cortex 16:313–20
   PubMed Web of Science ®Google Scholar
• Sandi C, Davies HA, Cordero MI, Rodriguez JJ, Popov VI, Stewart MG. (2003). Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur J Neurosci 17:2447–56
   PubMed Web of Science ®Google Scholar
• Selye HA. (1956). Syndrome produced by diverses nocuous agents. Nature 138:132
   Google Scholar
• Sicilia AG, Martínez AMA, Valenzuela PA, González Z MA, Granados RL, Barragán MMG. (2007). Efecto protector del pirofosfato de tiamina en el hipocampo de ratas expuestas a estrés por inmovilización forzada. Vet Méx 38(4):429–38
   Google Scholar
• Silva-Gómez AB, Aguilar-Salgado Y, Reyes-Hernández DO, Flores G. (2013). Dexamethasone induces different morphological changes in the dorsal and ventral hippocampus of rats. J Chem Neuroanat 47:71–8
   PubMed Web of Science ®Google Scholar
• Silva-Gómez AB, Rojas D, Juárez I, Flores G. (2003). Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983:128–36
   PubMed Web of Science ®Google Scholar
• Stewart J, Kolb B. (1994). Dendritic branching in cortical pyramidal cells in response to ovariectomy in adult female rats: suppression by neonatal exposure to testosterone. Brain Res 654:149–54
   PubMed Web of Science ®Google Scholar
• Sutcliffe JS, Marshall KM, Neill JC. (2007). Influence of sex on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 177:117–25
   PubMed Web of Science ®Google Scholar
• Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–18
   PubMed Web of Science ®Google Scholar
• Wallace M, Luine V, Arellanos A, Frankfurt M. (2006). Ovariectomized rats show decreased recognition memory and spine density in the hippocampus and prefrontal cortex. Brain Res 1126:176–82
   PubMed Web of Science ®Google Scholar
• Watanabe Y, Gould E, McEwen BS. (1992). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341–5
   PubMed Web of Science ®Google Scholar
• Woolley CS, Gould E, Frankfurt M, McEwen BS. (1990). Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10(12):4035–9
   PubMed Web of Science ®Google Scholar
• Woolley CS, McEwen BS. (1993). Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293–306
   PubMed Web of Science ®Google Scholar
• Woolley CS, McEwen BS. (1994). Estradiol regulates hippocampal dendritic spine density via an N-Methyl-D-Aspartate receptor-dependent mechanism. J Neurosci 14(12):7680–7
   PubMed Web of Science ®Google Scholar