Effects of prenatal stress and exercise on dentate granule cells maturation and spatial memory in adolescent mice

International Journal of Developmental Neuroscience

Volumn 28, Issue 7, 2010, Pages 605-609

  Bustamante, Carlos ^a   Bilbao, Pamela ^a   Contreras, William ^a   Martínez, Mauricio ^a   Mendoza, Antonio ^a   Reyes, Álvaro ^a   Pascual, Rodrigo ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE VALPARAÍSO   (Chile)

Author keywords

Dentate granule cells; Morris water maze; Prenatal stress; Voluntary wheel running

Indexed keywords

ADOLESCENT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; DENTATE GYRUS; EXERCISE; GRANULE CELL; MALE; MAZE TEST; MOUSE; NONHUMAN; PERINATAL PERIOD; PRENATAL STRESS; PRIORITY JOURNAL; SPATIAL MEMORY;

ANIMALS; DENDRITES; FEMALE; HIPPOCAMPUS; MALE; MEMORY; MICE; MOTOR ACTIVITY; NEURONS; NEUROPSYCHOLOGICAL TESTS; PHYSICAL CONDITIONING, ANIMAL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION; STRESS, PHYSIOLOGICAL;

ANIMALIA; MUS;

EID: 79961143085     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2010.07.229     Document Type: Article

References (50)

1. Adlard P.A., Perreau V.M., Pop V., Cotman C.W. Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J. Neurosci. 2005, 25:4217-4221.
2. Altman J., Bayer S.A. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J. Comp. Neurol. 1990, 301:365-381.
3. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995, 15:961-973.
4. Barros V.G., Duhalde-Vega M., Caltana L., Brusco A., Antonelli M.C. Astrocyte-neuron vulnerability to prenatal stress in the adult rat brain. J. Neurosci. Res. 2006, 83:787-800.
5. Berchtold N.C., Chinn G., Chou M., Kesslak J.P., Cotman C.W. Exercise primes a molecular memory for brain-derived neurotrophic factor protein induction in the rat hippocampus. Neuroscience 2005, 133:853-861.
6. Brandeis R., Brandys Y., Yehuda S. The use of the Morris water maze in the study of memory and learning. Int. J. Neurosci. 1989, 48:29-69.
7. Christie B.R., Swann S.E., Fox C.J., Froc D., Lieblich S.E., Redila V., Webber A. Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. Eur. J. Neurosci. 2005, 21:1719-1726.
8. Coe C.L., Kramer M., Czéh B., Gould E., Reeves A.J., Kirschbaum C., Fuchs E. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol. Psychiatry 2003, 54:1025-1034.
9. Cotman C.W., Berchtold N.C., Christie L.A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 2007, 30:464-472.
10. Diaz R., Fuxe K., Ogren S.O. Prenatal corticosterone treatment induces long-term changes in spontaneous and apomorphine-mediated motor activity in male and female rats. Neuroscience 1997, 81:129-140.
11. Ding Q., Vaynman S., Akhavan M., Ying Z., Gomez-Pinilla F. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 2006, 140:823-833.
12. Eadie B.D., Redila V.A., Christie B.R. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J. Comp. Neurol. 2005, 486:39-47.
13. Farmer J., Zhao X., Van Praag H., Wodtke K., Gage F.H., Christie B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004, 124:71-79.
14. Griesbach G.S., Hovda D.A., Molteni R., Wu A., Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor up regulation and recovery of function. Neuroscience 2004, 25:129-139.
15. Horner H., Packan D.A., Sapolsky R. Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. Neuroendocrinology 1990, 52:57-64.
16. Hosseini-Sharifabad M., Hadinedoushan H. 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. 2007, 82:211-217.
17. Huizink A.C., Mulder E.J.H., Buitelaar J.K. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?. Psychol. Bull. 2004, 130:115-142.
18. Huttenlocher P.R. Synaptic density in human frontal cortex-developmental changes and effects of aging. Brain Res. 1979, 163:195-205.
19. Jia N., Yang K., Sun Q., Cai Q., Li H., Cheng D., Fan X., Zhu Z. Prenatal stress causes dendritic atrophy of pyramidal neurons in hippocampal CA3 region by glutamate in offspring rats. Dev. Neurobiol. 2010, 70:114-125.
20. Louvart H., Maccari S., Darnaudéry M. Prenatal stress affects behavioral reactivity to an intense stress in adult female rats. Brain Res. 2005, 1031:67-73.
21. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A.R., Cinque C., Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 2003, 27:119-127.
22. Mainen Z.F., Sejnowski T.J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 1996, 382:363-366.
23. Malaspina D., Corcoran C., Kleinhaus K.R., Perrin M.C., Fennig S., Hahon D., Friedlander Y., Harlap S. Acute maternal stress in pregnancy and schizophrenia in offspring: a cohort prospective study. BMC Psychiatry 2008, 8:71-79.
24. Moore C.L., Power K.L. Prenatal stress affects mother-infant interaction in Norway rats. Dev. Psychobiol. 1986, 19:235-245.
25. Morley-Fletcher S., Rea M., Maccari S., Laviola G. Environmental enrichment during adolescence reverses the effects of prenatal stress on play behavior and HPA axis reactivity in rats. Eur. J. Neurosci. 2003, 18:3367-3374.
26. Murakami S., Imbe H., Morikawa Y., Kubo C., Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci. Res. 2005, 53:129-139.
27. O'Connor T.G., Heron J., Golding J., Glover V. Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. J. Child Psychol. Psychiatry 2003, 44:1025-1036.
28. Oliff H.S., Berchtold N.C., Isackson P., Cotman C.W. Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus. Mol. Brain Res. 1998, 61:147-153.
29. Patin V., Lordi B., Vincent A., Thoumas J.L., Vaudry H., Caston J. Effects of prenatal stress on maternal behavior in the rat. Dev. Brain Res. 2002, 139:1-8.
30. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, New York. fourth ed.
31. Redila V.A., Christie B.R. Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 2006, 137:1299-1307.
32. Sánchez M.M., Ladd C.O., Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 2001, 13:419-449.
33. Seckl J.R., Meaney M.J. Glucocorticoid programming. Ann. N.Y. Acad. Sci. 2004, 1032:63-84.
34. Sholl D. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 1953, 87:387-407.
35. Smith M.A., Makino S., Kvetnansky R., Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci. 1995, 15:1768-1777.
36. Son G.H., Geum D., Chung S., Kim E.J., Jo J.H., Kim C.M., Lee K.H., Kim H., Choi S., Kim H.T., Lee C.J., Kim K. Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J. Neurosci. 2006, 26:3309-3318.
37. Szuran T.F., Pliska V., Pokorny J., Welzl H. Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol. Behav. 2000, 71:353-362.
38. Takahashi L. Prenatal stress: consequences of glucocorticoids on hippocampal development and function. Int. J. Dev. Neurosci. 1998, 16:199-207.
39. Uylings H.B., Ruiz-Marcos A., van Pelt J. The metric analysis of three-dimensional dendritic tree patterns: a methodological review. J. Neurosci. Methods 1986, 18:127-151.
40. Van den Bergh B.R., Van Calster B., Smits T., Van Huffel S., Lagae L. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 2008, 33:536-545.
41. Van den Hove D.L.A., Blanco C.E., Aendekerk B., Desbonnet L., Bruschettini M., Steinbusch H.P., Prickaerts J., Steinbusch H.W. Prenatal restraint stress and long-term affective consequences. Dev. Neurosci. 2005, 27:313-320.
42. Van der Borght K., Kóbor-Nyakas D.E., Klauke K., Eggen B.J., Nyakas C., Van der Zee E.A., Meerlo P. Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 2009, 19:928-936.
43. Vaynman S., Ying Z., Gómez-Pinilla F. Exercise induces BDNF and synapsin I to specific hippocampal subfields. J. Neurosci. Res. 2004, 76:356-362.
44. Vaynman S., Gomez-Pinilla F. License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil. Neural Repair 2005, 19:283-295.
45. Virgin C.E., Ha T.P., Packan D.R., Tombaugh G.C., Yang S.H., Horner H.C., Sapolsky R.M. Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J. Neurochem. 1991, 57:1422-1428.
46. Wu J., Song T.B., Li Y.J., He K.S., Ge L., Wang L.R. Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats. Brain Res. 2007, 1141:205-213.
47. Yang J., Li W., Liu X., Li Z., Li H., Yang G., Xu L., Li L. Enriched environment treatment counteracts enhanced addictive and depressive-like behavior induced by prenatal chronic stress. Brain Res. 2006, 1125:132-137.
48. Yang J., Hou C., Ma N., Liu J., Zhang Y., Zhou J., Xu L., Li L. Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiol. Learn. Mem. 2007, 87:257-263.
49. Yaka R., Salomon S., Matzner H., Weinstock M. Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behav. Brain Res. 2007, 179:126-132.
50. You J.M., Yun S.J., Nam K.N., Kang Ch., Won R., Lee E.H. Mechanism of glucocorticoid-induced oxidative stress in rat hippocampal slice cultures. Can. J. Physiol. Pharmacol. 2009, 87:440-447.