Effect of exercise on learning and memory in a rat model of developmental stress

Metabolic Brain Disease

Volumn 24, Issue 4, 2009, Pages 643-657

  Grace, Laurian ^a   Hescham, Sarah ^a   Kellaway, Lauriston A ^a   Bugarith, Kishor ^a   Russell, Vivienne A ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Exercise; Learning and memory; Maternal separation; Stress

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXERCISE; EXPERIMENTAL MODEL; HIPPOCAMPUS; LEARNING; LIFE STRESS; MALE; MATERNAL DEPRIVATION; MAZE TEST; MEMORY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPEN FIELD BEHAVIOR; RAT; RECOGNITION; RUNNING; SPATIAL MEMORY; TASK PERFORMANCE;

ANIMALS; ANIMALS, NEWBORN; ANXIETY DISORDERS; DISEASE MODELS, ANIMAL; EXERCISE THERAPY; LEARNING; LEARNING DISORDERS; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; MEMORY; MEMORY DISORDERS; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TESTS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); STRESS, PSYCHOLOGICAL;

ANIMALIA; ELAGATIS; RATTUS;

EID: 74449091526     PISSN: 08857490     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11011-009-9162-5     Document Type: Article

References (45)

1. B Aisa R Tordera B Lasheras J Del Rio MJ Ramirez 2007 Cognitive impairment associated to HPA axis hyperactivity after maternal separation Psychoneuroendocrinology 32 256 266 10.1016/j.psyneuen.2006.12.013 1:CAS:528:DC%2BD2sXjtVegsr0%3D 17307298 (Pubitemid 46400278)
2. SL Andersen MH Teicher 2004 Delayed effects of early stress on hippocampal development Neuropsychopharmacology 29 1988 1993 10.1038/sj.npp.1300528 15316569 (Pubitemid 39486550)
3. GRI Barker F Bird V Alexander EC Warburton 2007 Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex J Neurosci 27 2948 2957 10.1523/JNEUROSCI.5289-06.2007 1:CAS:528:DC%2BD2sXjs1ajsro%3D 17360918 (Pubitemid 46438982)
4. V Bertaina-Anglade E Enjuanes D Morillon D la Rochelle 2006 The object recognition task in rats and mice: a simple and rapid model in safety pharmacology to detect amnesic properties of a new chemical entity J Pharmacol Toxicol Methods 54 99 105 10.1016/j.vascn.2006.04.001 1:CAS:528: DC%2BD28XptFChtbk%3D 16750402 (Pubitemid 44308867)
5. RA Bevins J Besheer 2006 Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory' Nature Protocols 1 1306 1311 10.1038/nprot.2006.205 17406415
6. E Binder SK Droste F Ohl JM Reul 2004 Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice Behav Brain Res 155 197 206 10.1016/j.bbr.2004.04.017 15364478 (Pubitemid 39208901)
7. PJ Clark WJ Brzezinska MW Thomas NA Ryzhenko SA Toshkov JS Rhodes 2008 Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice Neuroscience 155 1048 1058 10.1016/j.neuroscience.2008.06.051 1:CAS:528:DC%2BD1cXhtVKlsLbO 18664375
8. KM Clements AJ Saunders BA Robertson PE Wainwright 2007 Spontaneously hypertensive, Wistar Kyoto and Sprague-Dawley rats differ in their use of place and response strategies in the water radial arm maze Neurobiol Learn Mem 87 285 294 10.1016/j.nlm.2006.09.003 1:STN:280:DC%2BD2s%2FhslOqtQ%3D%3D 17056285 (Pubitemid 46038957)
9. MA Coleman T Garland CA Marler SS Newton JG Swallow PA Carter 1998 Glucocorticoid response to forced exercise in laboratory house mice (Mus domesticus) Physiol Behav 63 279 285 10.1016/S0031-9384(97)00441-1 1:CAS:528:DyaK2sXnvFWlu70%3D 9423970 (Pubitemid 28034081)
10. WMU Daniels CY Pietersen ME Carstens DJ Stein 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 1/2
11. CH Duman L Schlesinger DS Russell RS Duman 2008 Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice Brain Res 1199 148 158 1:CAS:528:DC%2BD1cXjtVWlsrY%3D 18267317
12. J Faure JDK Uys L Marais DJ Stein WMU Daniels 2007 Early maternal separation alters the response to traumitization: resulting in increased levels of hippocampal neurotrophic factors Metab Brain Dis 22 183 195 10.1007/s11011-007-9048-3 17468977 (Pubitemid 46985778)
13. MG Gareau J Jury MH Perdue 2007 Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability Am J Physiol Gastrointest Liver Physiol 293 198 203 10.1152/ajpgi.00392.2006
14. F Gomez-Pinilla S Vaynman 2005 A "deficient environment" in prenatal life may compromise systems important for cognitive function by affecting BDNF in the hippocampus Exp Neurol 192 235 243 10.1016/j.expneurol. 2004.12.001 1:CAS:528:DC%2BD2MXhvF2msrY%3D 15755541 (Pubitemid 40341671)
15. GS Griesbach DA Hovda R Molteni A Wu F Gomez-Pinnilla 2004 Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function Neuroscience 125 129 139 10.1016/j.neuroscience.2004.01.030 1:CAS:528:DC%2BD2cXisFyls7k%3D 15051152 (Pubitemid 38402166)
16. M Gruss K Braun JU Frey V Korz 2008 Maternal separation during a specific postnatal time window prevents reinforcement of the hippocampal long-term potentiation in adolescent rats Neuroscience 152 1 7 10.1016/j.neuroscience. 2007.12.033 1:CAS:528:DC%2BD1cXivVOls7s%3D 18255235
17. KM Horvath T Harkany J Mulder JM Koolhaas PG Luiten P Meerlo 2004 Neonatal handling increases sensitivity to acute neurodegeneration in adult rats J Neurobiol 60 463 472 10.1002/neu.20037 15307150 (Pubitemid 39108886)
18. FM Howells VA Russell MV Mabandla LA Kellaway 2005 Stress reduces the neuroprotective effect of exercise in a rat model for Parkinson's disease Behav Brain Res 165 210 220 10.1016/j.bbr.2005.06.044 1:CAS:528:DC%2BD2MXhtFylu7%2FO 16159673 (Pubitemid 41565531)
19. MR Hunsaker B Lee RP Kesner 2008 Evaluating the temporal context of episodic memory: the role of CA3 and CA1 Behav Brain Res 188 310 315 10.1016/j.bbr.2007.11.015 1:CAS:528:DC%2BD1cXhslOjtbc%3D 18178264
20. M Kalinichev KW Easterling PM Plotsky SG Holtzman 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)00781-5 1:CAS:528: DC%2BD38XksFKksbo%3D 12076732 (Pubitemid 34667025)
21. Kandel ER, Shwartz JH, Jessell TM (2006) Principals of neural science. McGraw-Hill, United States
22. RG Kathol RS Jaeckle JF Lopez WH Meller 1989 Pathophsiology of HPA axis abnormalities in patients with major depression: an update Am J Psychiatry 146 311 317 1:STN:280:DyaL1M7kvVCqtw%3D%3D 2645793
23. ED Knuth AM Etgen 2007 Long-term behavioral consequences of brief, repeated neonatal isolation Brain Res 1128 139 147 10.1016/j.brainres.2006.10. 054 1:CAS:528:DC%2BD2sXls1WgsQ%3D%3D 17125746 (Pubitemid 46055240)
24. I Lee 2005 The role of hippocampal subregions in detecting spatial novelty Behav Neurosci 119 145 153 10.1037/0735-7044.119.1.145 15727520 (Pubitemid 40279505)
25. D Liu J Diorio JC Day DD Francis MJ Meaney 2000 Maternal care, hippocampal synaptogenesis and cognitive development in rats Nat Neurosci 3 799 806 10.1038/77702 1:CAS:528:DC%2BD3cXlsVOlsbk%3D 10903573 (Pubitemid 30485705)
26. S Macri F Chiarotti H Wurbel 2008 Maternal separation and maternal care act independently on the development of HPA responses in male rats Behav Brain Res 191 227 234 10.1016/j.bbr.2008.03.031 1:CAS:528:DC%2BD1cXmtlSgtr8%3D 18468700
27. C Madruga LL Xavier M Achaval GL Sanvitto AB Lucion 2006 Early handling, but not maternal separation, decreases emotional responses in two paradigms of fear without changes in mesolimbic dopamine Behav Brain Res 166 241 246 10.1016/j.bbr.2005.08.005 1:CAS:528:DC%2BD2MXhtlajt7bM 16171878 (Pubitemid 41785369)
28. L Marais SJ van Rensburg JM van Zyl DJ Stein WMU Daniels 2008 Maternal separation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus Neurosci Res 61 106 112 10.1016/j.neures.2008.01.011 1:CAS:528:DC%2BD1cXkvVOqu70%3D 18329744
29. M Marmendal CJP Erkisson C Fahlke 2006 Early deprivation increases exploration and locomotion in adult male Wistar offspring Pharmacol Biochem Behav 85 535 544 10.1016/j.pbb.2006.10.005 1:CAS:528:DC%2BD2sXnslGqtA%3D%3D 17109940 (Pubitemid 46097064)
30. PB Mello F Benetti M Cammarota I Izquierdo 2008 Effects of acute and chronic physical exercise and stress on different types of memory in rats Anais da Academia Brasilera de Ciencias 80 301 309
31. AR Mesquita JM Pego T Summaveille P Maciel OFX Almeida N Sousa 2007 Neurodevelopment milestone abnormalities in rats exposed to stress in early life Neuroscience 147 1022 1033 10.1016/j.neuroscience.2007.04.007 1:CAS:528:DC%2BD2sXotlSltL0%3D 17587501
32. C Pickering L Gustafsson A Cebere I Nylander S Liljequist 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.2006.04.136 1:CAS:528:DC%2BD28XntlWit7Y%3D 16784730 (Pubitemid 44080106)
33. L Prut C Belzung 2003 The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review Eur J Pharmacol 463 3 33 10.1016/S0014-2999(03)01272-X 1:CAS:528:DC%2BD3sXhsVanu70%3D 12600700 (Pubitemid 36205070)
34. M Roceri W Hendricks G Racagni BA Ellenbroek MA Riva 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.4001036 1:CAS:528: DC%2BD38XlsFWrsbo%3D 12140784 (Pubitemid 34888424)
35. AM Stranahan D Khalil E Gould 2006 Social isolation delays the positive effects of running on adult neurogenesis Nat Neurosci 9 526 533 10.1038/nn1668 1:CAS:528:DC%2BD28XivFSiur4%3D 16531997
36. AM Stranahan D Khalil E Gould 2007 Running induces widespread structural alterations in the hippocampus and the entorhinal cortex Hippocampus 17 1017 1022 10.1002/hipo.20348 17636549 (Pubitemid 350156815)
37. AC Tang BC Reeb RD Romeo BS McEwen 2003 Modification of social memory, hypothalamic-pituitary-adrenal axis, and brain asymmetry by neonatal novelty exposure J Neurosci 23 8254 8260 1:CAS:528:DC%2BD3sXnsVGgurk%3D 12967987
38. M Vallee W Mayo F Dellu M Le Moal H Simon S Maccari 1997 Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion J Neurosci 7 2626 2636
39. S Vaynman Z Ying F Gomez-Pinilla 2004 Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition Eur J NeuroSci 20 2580 2590 10.1111/j.1460-9568.2004.03720.x 15548201 (Pubitemid 39573773)
40. S Vaynman Z Ying F Gomez-Pinilla 2007 The select action of hippocampal calcium calmodulin protein kinase II in mediating exercise-enhanced cognitive function Neuroscience 144 825 833 10.1016/j.neuroscience.2006.10.005 1:CAS:528:DC%2BD2sXhsFKrsg%3D%3D 17161914 (Pubitemid 46013982)
41. CV Vorhees MT Williams 2006 Morris water maze: procedures for assessing spatial and related forms of learning and memory Nature Protocols 1 848 858 10.1038/nprot.2006.116 17406317
42. AA Walf CA Frye 2007 The use of the elevated plus maze as an assay of anxiety-related behavior in rodents Nature Protocols 2 322 328 10.1038/nprot.2007.44 1:CAS:528:DC%2BD2sXhtFGntbvP 17406592 (Pubitemid 47040046)
43. J Widenfalk L Olson P Thoren 1999 Deprived of habitual running, rats down-regualte BDNF and TrkB messages in the brain Neurosci Res 34 125 132 10.1016/S0168-0102(99)00051-6 1:CAS:528:DyaK1MXlvVWrtrw%3D 10515254 (Pubitemid 29421716)
44. A Wigger ID Neumann 1999 Gender-Dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats Physiol Behav 66 293 302 10.1016/S0031-9384(98)00300-X 1:CAS:528:DyaK1MXjtFGmtL8%3D 10336157 (Pubitemid 29206522)
45. Z Ying RR Roy H Zhong S Zdunowski VR Edgerton F Gomez-Pinilla 2008 BDNF-exercise interactions in the recovery of symmetrical stepping after a cervical hemisection in rats Neuroscience 155 1070 1078 10.1016/j.neuroscience. 2008.06.057 1:CAS:528:DC%2BD1cXhtVKlsLbI 18672032