2011, Number 3
<< Back Next >>
Rev Invest Clin 2011; 63 (3)
Intrauterine stress impairs spatial learning in the progeny of Wistar rats
Gonzalez-Perez O, Gutiérrez-Smith Y, Guzmán-Muñiz J, Moy-López NA
Language: Spanish
References: 55
Page: 279-286
PDF size: 138.88 Kb.
ABSTRACT
Introduction. Prenatal stress is a group of psychophysiological
responses that a pregnant female shows when confronting
by a threatening situation. This produces neurochemical
changes that may affect hippocampal development of the offspring.
Aim. To analyze the effects of intrauterine stress on
spatial learning and memory of Wistar rat offspring.
Material
and methods. Wistar rats were divided in two groups:
Control and prenatal stress. During the critical period for the
development of the central nervous system development (from
day 12 to 18 of gestation), the experimental rats were exposed
to prenatal stress using a restraint stress model. Control rats
were kept under standard housing conditions. At 21-days postpartum,
spatial learning and memory were evaluated with
the Morris water maze.
Results. Intrauterine-stressed offspring
showed less weight gain (62.7 ± 11.7 g) compared to
controls (71.3 ± 7.4 g; t
(42) = 2.87; P = 0.006). Spatial learning
assessment indicated that intrauterine-stressed animals
showed higher escape latencies (63 ± 14 s) than the control
group (49 ± 13 seg; t
(42) = 3.2, P = 0.003). The navigation pattern
of the stress group was allocentric as compared to the
egocentric strategy shown by controls. No significant statistical
differences were found in memory consolidation.
Conclusions.
Intrauterine stress impairs hippocampal function
during postnatal development. The knowledge of deleterious
effects of intrauterine stress may be helpful in establishing
primary prevention strategies of pregnant women exposed to
this risk factor.
REFERENCES
Seaward BL. The stress of life: Selye, Jung, Taylor & you. Beginnings 2007; 27(1): 4-5.
Zurroza-Estrada AD, Oviedo-Rodriguez IJ, Ortega-Gomez R, Gonzalez-Perez O. Relationship between personality profiles and stress in medical residents. Rev Invest Clin 2009; 61(2): 110-8.
McEwen BS. The neurobiology and neuroendocrinology of stress. Implications for post-traumatic stress disorder from a basic science perspective. Psychiatr Clin North Am 2002; 25(2): 469-94, ix.
McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 2007; 87(3): 873-904.
Weinstock M. Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci Biobehav Rev 1997; 21(1): 1-10.
Vallee M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 1997; 17(7): 2626-36.
Tronche C, Pierard C, Coutan M, Chauveau F, Liscia P, Beracochea D. Increased stress-induced intra-hippocampus corticosterone rise associated with memory impairments in middle-aged mice. Neurobiol Learn Mem 2010; 93(3): 343-51.
Kim JJ, Song EY, Kosten TA. Stress effects in the hippocampus: synaptic plasticity and memory. Stress 2006; 9(1): 1-11.
Brown ES. Effects of glucocorticoids on mood, memory, and the hippocampus. Treatment and preventive therapy. Ann NY Acad Sci 2009; 1179: 41-55.
Aisa B, Elizalde N, Tordera R, Lasheras B, Del Rio J, Ramirez MJ. Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory. Hippocampus 2009; 19(12): 1222-31.
Jauregui-Huerta F, Ruvalcaba-Delgadillo Y, Gonzalez-Castaneda R, Garcia-Estrada J, Gonzalez-Perez O, Luquin S. Responses of glial cells to stress and glucocorticoids. Curr Immunol Rev 2010; 6(3): 195-204.
Venero C, Borrell J. Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. Eur J Neurosci 1999; 11(7): 2465-73.
Stein-Behrens BA, Lin WJ, Sapolsky RM. Physiological elevations of glucocorticoids potentiate glutamate accumulation in the hippocampus. J Neurochem 1994; 63(2): 596-602.
Moghaddam B, Bolinao ML, Stein-Behrens B, Sapolsky R. Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res 1994; 655(1-2): 251-4.
Karst H, Berger S, Turiault M, Tronche F, Schutz G, Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA 2005; 102(52): 19204-07.
De Kloet ER, Karst H, Joels M. Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 2008; 29(2): 268-72.
Olijslagers JE, De Kloet ER, Elgersma Y, Van Woerden GM, Joels M, Karst H. Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci 2008; 27(10): 2542-50.
Tasker JG, Di S, Malcher-Lopes R. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 2006; 147(12): 5549-56.
Sembulingam K, Sembulingam P, Namasivayam A. Effect of acute noise stress on acetylcholinesterase activity in discrete areas of rat brain. Indian J Med Sci 2003; 57(11): 487-92.
Bautista A, Garcia-Torres E, Prager G, Hudson R, Rodel HG. Development of behavior in the litter huddle in rat pups: within- and between-litter differences. Dev Psychobiol 2010; 52(1): 35-43.
Champagne F, Meaney MJ. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 2001; 133: 287-302.
Champagne F, Diorio J, Sharma S, Meaney MJ. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 2001; 98(22): 12736-41.
Buynitsky T, Mostofsky DI. Restraint stress in biobehavioral research: Recent developments. Neurosci Biobehav Rev 2009; 33(7): 1089-98.
Klenerova V, Krejci I, Sida P, Hlinak Z, Hynie S. Modulary effects of oxytocin and carbetocin on stress-induced changes in rat behavior in the open-field. J Physiol Pharmacol 2009; 60(2): 57-62.
Paxinos G. The rat nervous system. 3rd ed. San Diego, CA: Elsevier Academic Press; 2004.
Moscovitch M, Rosenbaum RS, Gilboa A, et al. Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 2005; 207(1): 35-66.
Van der Staay FJ. Assessment of age-associated cognitive deficits in rats: a tricky business. Neurosci Biobehav Rev 2002; 26(7): 753-9.
Mulder GB, Pritchett K. The Morris water maze. Contemp Top Lab Anim Sci 2003; 42(2): 49-50.
Ramos-Remus C, Gonzalez-Castaneda RE, Gonzalez-Perez O, Luquin S, Garcia-Estrada J. Prednisone induces cognitive dysfunction, neuronal degeneration, and reactive gliosis in rats. J Investig Med 2002; 50(6): 458-64.
Igloi K, Zaoui M, Berthoz A, Rondi-Reig L. Sequential egocentric strategy is acquired as early as allocentric strategy: Parallel acquisition of these two navigation strategies. Hippocampus 2009; 19(12): 1199-211.
Begega A, Cienfuegos S, Rubio S, Santin JL, Miranda R, Arias JL. Effects of ageing on allocentric and egocentric spatial strategies in the Wistar rat. Behav Processes 2001; 53(1-2): 75-85.
Gould E, Tanapat P. Stress and hippocampal neurogenesis. Biol Psychiatry 1999; 46(11): 1472-9.
Gould E, Tanapat P, Rydel T, Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry 2000; 48(8): 715-20.
Segal M, Richter-Levin G, Maggio N. Stress-induced dynamic routing of hippocampal connectivity: A hypothesis. Hippocampus 2010.
Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 1992; 12(9): 3642-50.
Rodriguez JJ, Montaron MF, Petry KG, et al. Complex regulation of the expression of the polysialylated form of the neuronal cell adhesion molecule by glucocorticoids in the rat hippocampus. Eur J Neurosci 1998; 10(9): 2994-3006.
Montaron MF, Petry KG, Rodriguez JJ, et al. Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus. Eur J Neurosci 1999; 11(4): 1479-85.
Warner A, Ovadia H, Tarcic N, Weidenfeld J. The effect of restraint stress on glucocorticoid receptors in mouse spleen lymphocytes: involvement of the sympathetic nervous system. Neuroimmunomodulation 2010; 17(5): 298-304.
Rogalska J. Mineralocorticoid and glucocorticoid receptors in hippocampus: their impact on neurons survival and behavioral impairment after neonatal brain injury. Vitam Horm 2010; 82: 391-419.
Beaumont K, Fanestil DD. Characterization of rat brain aldosterone receptors reveals high affinity for corticosterone. Endocrinology 1983; 113(6): 2043-51.
Van Eekelen JA, De Kloet ER. Co-localization of brain corticosteroid receptors in the rat hippocampus. Prog Histochem Cytochem 1992; 26(1-4): 250-8.
Wrange O, Yu ZY. Mineralcorticoid receptor in rat kidney and hippocampus: characterization and quantitation by isoelectric focusing. Endocrinology 1983; 113(1): 243-50.
Nelson DL, Schreiber TA, McEvoy CL. Processing implicit and explicit representations. Psychol Rev 1992; 99(2): 322-48.
Conrad CD, Bimonte-Nelson HA. Impact of the hypothalamicpituitary- adrenal/gonadal axes on trajectory of age-related cognitive decline. Prog Brain Res 2010; 182: 31-76.
Joels M. Impact of glucocorticoids on brain function: Relevance for mood disorders. Psychoneuroendocrinol 2010.
Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996; 16(6): 2027-33.
Sapolsky RM, Krey LC, McEwen BS. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 1985; 5(5): 1222-7.
Gonzalez-Castaneda RE, Castellanos-Alvarado EA, Flores- Marquez MR, et al. Deflazacort induced stronger immunosuppression than expected. Clin Rheumatol 2007; 26(6): 935-40.
Gonzalez-Perez O, Luquin S, Garcia-Estrada J, Ramos-Remus C. Deflazacort: a glucocorticoid with few metabolic adverse effects but important immunosuppressive activity. Adv Ther 2007; 24(5): 1052-60.
Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000; 97(20): 11032-7.
Gonzalez-Perez O, Ramos-Remus C, Garcia-Estrada J, Luquin S. Prednisone induces anxiety and glial cerebral changes in rats. J Rheumatol 2001; 28(11): 2529-34.
Seki T, Arai Y. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 1995; 6(18): 2479-82.
Son GH, Geum D, Chung S, et al. Maternal stress produces learning deficits associated with impairment of NMDA receptor- mediated synaptic plasticity. J Neurosci 2006; 26(12): 3309-18.
Hayashi A, Nagaoka M, Yamada K, Ichitani Y, Miake Y, Okado N. Maternal stress induces synaptic loss and developmental disabilities of offspring. Int J Dev Neurosci 1998; 16(3-4): 209-16.
Lanzenberger R, Wadsak W, Spindelegger C, et al. Cortisol plasma levels in social anxiety disorder patients correlate with serotonin-1A receptor binding in limbic brain regions. Int J Neuropsychopharmacol 2010: 1-15.