Physical exercise can reverse the deficit in fear memory induced by maternal deprivation

Neurobiology of Learning and Memory

Volumn 92, Issue 3, 2009, Pages 364-369

  Mello, Pâmela Billig ^a,b   Benetti, Fernando ^a,b   Cammarota, Martín ^a   Izquierdo, Iván ^a  

^a Instituto do Cérebro   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Learning; Maternal deprivation; Memory deficit; Treadmill running

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; COGNITIVE DEFECT; CONTROLLED STUDY; COPING BEHAVIOR; EXERCISE; FEMALE; LEARNING; LONG TERM MEMORY; MALE; MATERNAL DEPRIVATION; MAZE TEST; MEMORY DISORDER; NEUROENDOCRINE SYSTEM; NONHUMAN; OPEN FIELD BEHAVIOR; OXYGEN CONSUMPTION; RAT; RECOGNITION; SPATIAL MEMORY; TASK PERFORMANCE; TREADMILL EXERCISE;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; EXPLORATORY BEHAVIOR; FEAR; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; MEMORY; MEMORY DISORDERS; NEUROPSYCHOLOGICAL TESTS; OXYGEN CONSUMPTION; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; RECOGNITION (PSYCHOLOGY); SPACE PERCEPTION;

EID: 69249210972     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.04.004     Document Type: Article

References (61)

1. Aisa B., Tordera R., Laceras B., Del Río J., and Ramírez M.J. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32 (2007) 256-266
2. Alaei H., Borjeian L., Azizi M., Orian S., Pourshanazari A., and Hanninen O. Treadmill running reverses retention deficit induced by morphine. European Journal of Pharmacology 536 (2006) 138-141
3. Alaei H., Moloudi R., and Sarkaki A.R. Effects of treadmill running on mid-term memory and swim speed in the rat with Morris water maze test. Journal of Bodywork Movement Therapies 12 (2007) 72-75
4. Ang E.T., Dawe G.S., Wong P.T.H., Moochhala S., and Ng Y.K. Alterations in spatial learning and memory after forced exercise. Brain Research 1113 (2006) 186-193
5. Ang E.T., and Gomez-Pinilla F. Potential therapeutic effects of exercise to the brain. Current Medicinal Chemistry 14 (2007) 2564-2571
6. Ang E.T., Wong P.T.H., Moochhala S., and Ng Y.K. Neuroprotection associated with running: Is it a result of increased endogenous neurothrofic factors. Neuroscience 118 (2003) 335-345
7. Barnes C.A., Forster M.J., Fleshner M., Ahanotu E.N., Laudenslager M.L., Mazzeo R.S., et al. Exercise does not modify spatial memory, brain autoimmunity, or antibody response in aged F-344 rats. Neurobiology of Aging 12 (1991) 47-53
8. Benetti F., Andrade de Araújo P., Sanvitto G.L., and Lucion A.B. Effects of neonatal novelty exposure on sexual behavioural, fear, and stress-response in adult rats. Developmental Psycobiology 49 (2007) 258-264
9. Benetti F., Mello P.B., Monteiro S.C., Bonini J.S., Cammarota M., and Izquierdo I. Early postnatal maternal deprivation in rats induces cognitive impairment in adult life; the deficit is reversed by donepezil and galantamine. International Journal of Developmental Neuroscience 2 (2009) 59-64
10. Brooks G.A., and White T.P. Determination of metabolic and heart rate responses of rats in treadmill exercise. Journal of Applied Physiology 45 (1978) 1009-1015
11. Cammarota M., Bernabeu R., Izquierdo I., and Medina J.H. Reversible changes in hippocampal 3H-AMPA binding following inhibitory avoidance training in the rat. Neurobiology of Learning and Memory 66 (1996) 85-88
12. Campbell J.E., Rakhshani N., Fediuc S., Bruni S., and Riddell M.C. Voluntary wheel running initially increases adrenal sensitivity to adrenocorticotrophic hormone, which is attenuated with long-term training. Journal of Applied Physiology 106 (2008) 66-72
13. Chen H., Lin L., Yu L., Liu Y., Kuo Y., Huang A., et al. Treadmill exercise enhances passive avoidance learning in rats: The role of down-regulated serotonin system in the limbic system. Neurobiology of Learning and Memory 89 (2007) 489-496
14. Chirstie B.R., Swann S.E., Fox C.J., Froc D., Lieblich S.E., Redila V., et al. Voluntary exercise rescues deficits in spatial memory and long-term potention in prenatal ethanol-exposed male rats. European Journal of Neuroscience 21 (2005) 1719-1726
15. Cirulli F., Micera A., Alleva E., and Aloe L. Early maternal separation increases NGF expression in the developing rat hippocampus. Pharmacology Biochemistry and Behavior 59 (1998) 853-858
16. Cotman C.W., and Berchtold N.C. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends in Neuroscience 25 (2002) 295-301
17. Dishman R.K. Brain monoamines, exercise, and behavioral stress: Animals models. Medicine and Science in Sports and Exercise 29 (1997) 63-74
18. Dishman R.K., Renner K.J., Youngstedt S.D., Reigle T.G., Bunnell B.N., Burke K.A., et al. Activity wheel running reduces escape latency and alters monoamine levels after footshock. Brain Research Bulletin 42 (1997) 399-406
19. Droste S.K., Chandramohan Y., Hill L.E., Linthorst A.C.E., and Reual J.M.H.M. Voluntary exercise impacts on the rat hypothalamic-pituitary-adrenocortical axis mainly at the adrenal level. Neuroendocrinology 86 (2007) 26-37
20. Droste S.K., Gesing A., Ulbricht S., Müller M.B., Linthorst A.C., and Reul J.M.H.M. Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology 144 (2003) 3012-3023
21. Ennaucer A., and Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioral Brain Research 31 (1988) 47-59
22. Frick K.M., Stillner E.T., and Berger-Sweeney J. Mice are not little rats: Species differences in a one-day water maze task. NeuroReport 11 (2000) 3461-3465
23. Friedland R.P., Fritsch T., Smyth K.A., Koss E., Lerner A.J., Chen C.H., et al. Patients with Alzheimer's disease have reduced activities in midlife compared with healthy control-group members. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 3440-3445
24. Garza A.A., Ha T.G., Garcia C., Chen M.J., and Russo-Neustadt A. Exercise, antidepressant treatment, and BDNF mRNA expression in the aging brain. Pharmacology Biochemistry and Behavior 77 (2004) 209-220
25. Hout R.L., Plotsky P.M., Lenox R.H., and Mcnamara R.K. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Research 950 (2002) 52-63
26. Izquierdo I., Bevilaqua L.R., Rossato J.I., Bonini J.S., Medina J.H., and Cammarota M. Different molecular cascades in different sites of the brain control memory consolidation. Trends in Neuroscience 29 (2006) 496-505
27. Kennedy S.L., Smith T.P., and Fleshner M. Resting cellular and physiological effects of freewheel running. Medicine and Science in Sports and Exercise 37 (2005) 79-83
28. Kim H.G., Lim E.Y., Jung W.R., Shin M.K., Ann E.S., and Kim K.L. Effects of treadmill exercise on hipoactivity of the hypothalamo-pituitary-adrenal axis induced by chronic administration of corticosterione in rats. Neuroscience Letters 434 (2008) 46-49
29. Kosten T.A., Lee H.J., and Kim J.J. Neonatal handling alters learning in adult male and female rats in a task-specific manner. Brain Research 18 (2007) 144-153
30. Krugers H.J., Douma B.R., Andringa G., Bohus B., Korf J., and Luiten P.G. Exposure to chronic psychosocial stress and corticosterone in the rats: Effects on spatial discrimination learning and hippocampal protein kinase Cgamma immunoreactivity. Hippocampus 7 (1997) 427-436
31. Kuma H., Miki T., Matsumoto Y., Gu H., Li H.P., Kusaka T., et al. Early maternal deprivation induces alterations in brain-derived neurotrophic factor expression in the developing rat hippocampus. Neuroscience Letters 372 (2004) 68-73
32. Laurin D., Verreault R., Lindsay J., Macpherson K., and Rockwood K. Physical activity and risk of cognitive impairment and dementia in elderly persons. Archives of Neurology 58 (2001) 498-504
33. Lehmann J., Pryce C.R., Bettschen D., and Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacology Biochemistry and Behavior 64 (1999) 705-715
34. Liu D., Caldji C., Sharma S., Plotsky P.M., and Meaney M.J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and noreepinepherine release in the hypothalamic paraventricuar nucleus. Journal of Neuroendocrinology 12 (2000) 5-12
35. McGaugh J.L. The amygdale modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 27 (2004) 1-28
36. McIntosh J., Anisman H., and Merali Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: Gender-dependent effects. Brain Research 113 (1999) 97-106
37. Mello P.B., Benetti F., Cammarota M., and Izquierdo I. Effects of acute and chronic exercise and stress on different types of memory in rats. Anais da Academia Brasileira de Ciências 80 (2008) 301-309
38. Mirescu C., and Gould E. Stress and adult neurogenesis. Hippocampus 16 (2006) 233-238
39. Mitra, R., & Sapolsky, R.M. (in press). Effects of enrichment predominate over those of chronic stress on fear related behavior in male rats. Stress.
40. Moraska A., Deak T., Spencer R.L., Roth D., and Fleshner M. Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. American Journal of Physiology - Regulatory, Integrative Comparative Physiology 279 (2000) 321-329
41. Morris R.T., Fine D.M., Lees S.J., Booth F.W., Link C.D., Ferrario C.M., et al. Exercise training prevents development of cardiac contractile dysfunction in hypertensive TG (mREN-2)27 rats. Journal of the American Society of Hypertension 1 (2007) 393-399
42. Myskiw J.C., Rossato J.I., Bevilaqua L.R., Medina J.H., Izquierdo I., and Cammarota M. On the role of mTOR in recognition memory. Neurobiology of Learning and Memory 89 (2008) 338-351
43. Oitzl M.S., Workel J.O., Fluttert M., Frosch F., and de Kloet E.R. Maternal deprivation affects behavior from youth to senescence: Amplification of individual differences in spatial learning and memory in senescence Brown Norway rats. European Journal of Neuroscience 12 (2000) 3771-3780
44. Paratcha G., Furman M., Bevilaqua L., Cammarota M., Vianna M., de Stein M.l., et al. Involvement of hippocampal PKCbetaI isoform in the early phase of memory formation of an inhibitory avoidance learning. Brain Research 855 (2000) 199-205
45. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., and Meaney M.J. Long-term consequences of neonatal rearing on central corticotrophin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 30 (2005) 2192-2204
46. Radak Z., Told A., Szabo Z., Siamilis S., Nyakas C., Silye G., et al. The effects of training and detraining on memory, neurotrophins and oxidative stress markers in rat brain. Neurochemistry International 49 (2006) 387-392
47. Renard G.M., Suárez M.M., Levin G.M., and Rivarola M.A. Sex differences in rats: Effects of chronic stress on shympathetic system and anxiety. Physiology and Behavior 85 (2005) 363-369
48. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., and Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Molecular Psychiatry 7 (2002) 609-616
49. Rossato J.I., Bevilaqua L.R.M., Lima R.H., Medina J.H., Izquierdo I., and Cammarota M. On the participation of hippocampal p38 mitogen-activated protein kinase in extinction and reacquisition of inhibitory avoidance memory. Neuroscience 143 (2006) 15-23
50. Rossato J.I., Bevilaqua L.R.M., Medina J.H., and Cammarota M. Retrieval induces hippocampal-dependent reconsolidation of spatial memory. Learning and Memory 13 (2006) 431-440
51. Rossato J.I., Bevilaqua L.R.M., Myskiw J.C., Medina J.H., Izquierdo I., and Cammarota M. On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learning and Memory 14 (2007) 36-46
52. Rots N.Y., de Jong J., Workel J.O., Levine S., Cools A.R., and de Kloet E.R. Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibilty to apomorphine. Journal of Neuroendocrinology 8 (1996) 501-506
53. Schmidt M.Y., Oitzl M.S., Levine S., and de Kloet E.R. The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Brain Research Developmental Brain Research 139 (2002) 39-49
54. Scopel D., Fochesatto C., Cimarosti H., Rabbo M., Belló-Klein A., Salbego C., et al. Exercise intensity influences cell injury in rat hippocampal slices exposed to oxygen and glucose deprivation. Brain Research Bulletin 71 (2006) 155-159
55. Silva, S. G., Doná, F., Fernandes, M. J. S., Scorza, F. A., Cavalheiro, E. A., & Arida, R. M. (in press). Physical exercise during the adolescent period of life increases hippocampal parvalbumin expression. Brain and Development.
56. Simões P.A., Zamarioli A., Blóes P., Mazzocato F.C., Pereira L.H., Volpon J.B., et al. Effect of treadmill exercise on lumbar vertebrae in ovariectomized rats: Anthropometrical and mechanical analyses. Acta of Bioengineering and Biomechanics 10 (2008) 39-41
57. Todeschin, A. S., Winkelmann-Duarte, E. C., Jacob, M. H., Aranda, B. C., Jacobs, S., & Fernandes, M. C. et al. (in press). Effects of neonatal handling on social memory, social interaction, and number of oxytocin and vasopressin neurons in rats. Hormones and Behavior.
58. Uysal N., Tugyan K., Kayatekin B.M., Acikgoz O., Bagriyanik H.A., Gonenc S., et al. The effects of regular aerobic exercise in adolescent period on hippocampal neuron density, apoptosis and spatial memory. Neuroscience Letters 383 (2005) 241-245
59. Van Praag H., Shubert T., Ahao C., and Gage F. Exercise enhances learning and hippocampal neurogenesis in aged mice. Journal of Neuroscience 25 (2005) 8680-8685
60. Veena J., Srikumar B.N., Mahati K., Bhaga V., Raju T.R., and Shankaranarayana Rao B.S. Enriched environment restores hippocampal cell proliferation and ameliorates cognitive deficits in chronically stressed rats. Journal of Neuroscience Research 87 (2007) 831-843
61. Winter B., Breitenstein C., Mooren F.C., Voelker K., Fobker M., Lechtermann A., et al. High impact running improves learning. Neurobiology of Learning and Memory 87 (2007) 597-609