Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male sprague-dawley rats in vivo

Neuroscience

Volumn 124, Issue 1, 2004, Pages 71-79

  Farmer, J ^a   Zhao, X ^b   Van Praag, H ^b   Wodtke, K ^a   Gage, F H ^b   Christie, B R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 (2 CARBOXYPIPERAZIN 4 YL)PROPANEPHOSPHONIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMATE RECEPTOR 5; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; DENTATE GYRUS; DRUG ANTAGONISM; EXERCISE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; RAT STRAIN; THETA RHYTHM; TREADMILL; VOLUNTARY MOVEMENT;

EID: 0442307920     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2003.09.029     Document Type: Article

References (74)

1. Abraham W.C., Mason-Parker S.E., Bear M.F., Webb S., Tate W.P. Heterosynaptic metaplasticity in the hippocampus in vivo a BCM-like modifiable threshold for LTP . Proc Natl Acad Sci USA. 98:2001;10924-10929.
2. Aronica E., Frey U., Wagner M., Schroeder H., Krug M., Ruthrich H., Catania M.V., Nicoletti F., Reymann K.G. Enhanced sensitivity of metabotropic glutamate receptors after induction of long-term potentiation in rat hippocampus. J Neurochem. 57:1991;376-383.
3. Bartrup J.T., Moorman J.M., Newberry N.R. BDNF enhances neuronal growth and synaptic activity in hippocampal cell cultures. Neuroreport. 8:1997;3791-3794.
4. Berchtold N.C., Kesslak J.P., Cotman C.W. Hippocampal brain-derived neurotrophic factor gene regulation by exercise and the medial septum. J Neurosci Res. 68:2002;511-521.
5. Binder D.K., Croll S.D., Gall C.M., Scharfman H.E. BDNF and epilepsy too much of a good thing? Trends Neurosci. 24:2001;47-53.
6. Bland B.H. The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol. 26:1986;1-54.
7. Bland B.H., Oddie S.D. Theta band oscillation and synchrony in the hippocampal formation and associated structures the case for its role in sensorimotor integration . Behav Brain Res. 127:2001;119-136.
8. Bortolotto Z.A., Clarke V.R., Delany C.M., Parry M.C., Smolders I., Vignes M., Ho K.H., Miu P., Brinton B.T., Fantaske R., Ogden A., Gates M., Ornstein P.L., Lodge D., Bleakman D., Collingridge G.L. Kainate receptors are involved in synaptic plasticity. Nature. 402:1999;297-301.
9. Castellano C., Cestari V., Ciamei A. NMDA receptors and learning and memory processes. Curr Drug Targets. 2:2001;273-283.
10. Cameron H.A., Hazel T.G., McKay R.D. Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol. 36:1998;287-306.
11. Campbell I.G., Guinan M.J., Horowitz J.M. Sleep deprivation impairs long-term potentiation in rat hippocampal slices. J Neurophysiol. 88:2002;1073-1076.
12. Carro E., Nunez A., Busiguina S., Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci. 20:2000;2926-2933.
13. Christie B.R., Abraham W.C. NMDA-dependent heterosynaptic long-term depression in the dentate gyrus of anaesthetized rats. Synapse. 10:1992;1-6.
14. Christie B.R., Abraham W.C. Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron. 9:1992;79-84.
15. Clayton N.S., Krebs J.R. Hippocampal growth and attrition in birds affected by experience. Proc Natl Acad Sci. 91:1994;7410-7414.
16. Colino A., Malenka R.C. Mechanisms underlying induction of long-term potentiation in rat medial and lateral perforant paths in vitro. J Neurophysiol. 69:1993;1150-1159.
17. Collingridge G.L., Bliss T.V.P. Memories of NMDA receptors and LTP. Trends Neurosci. 18:1995;54-56.
18. del Rio J.A., Soriano E. Immunocytochemical detection of 5′-bromodeoxyuridine incorporation in the central nervous system of the mouse. Brain Res Dev Brain Res. 49:1989;311-317.
19. Duffy S.N., Craddock K.J., Abel T., Nguyen P.V. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus- dependent memory. Learn Mem. 8:2001;26-34.
20. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat Med. 4:1998;1313-1317.
21. Gomez-Pinilla F., Dao L., So V. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res. 764:1997;1-8.
22. Gooney M., Shaw K., Kelly A., O'Mara S.M., Lynch M.A. Long-term potentiation and spatial learning are associated with increased phosphorylation of TrkB and extracellular signal-regulated kinase (ERK) in the dentate gyrus evidence for a role for brain-derived neurotrophic factor . Behav Neurosci. 116:2002;455-463.
23. Gould E., Tanapat P., McEwen B.S. Adrenal steroids suppress granule cell death in the developing dentate gyrus through an NMDA receptor-dependent mechanism. Brain Res Dev Brain Res. 103:1997;91-93.
24. Gould E., Tanapat P., Hastings N.B., Shors T.J. Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA. 96:1999;5263-5267.
25. Gould E., Tanapat P., Rydel T., Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry. 48:2000;715-720.
26. Greenstein Y.J., Pavlides C., Winson J. Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity. Brain Res. 438:1988;331-334.
27. Hanse E., Gustafsson B. Long-term potentiation and field EPSPs in the lateral and medial perforant paths in the dentate gyrus in vitro a comparison . Eur J Neurosci. 4:1992;1191-1201.
28. Harvey B.H., Jonker L.P., Brand L., Heenop M., Stein D.J. NMDA receptor involvement in imipramine withdrawal-associated effects on swim stress, GABA levels and NMDA receptor binding in rat hippocampus. Life Sci. 71:2002;43-54.
29. Holscher C. Stress impairs performance in spatial water maze learning tasks. Behav Brain Res. 100:1999;225-235.
30. Jarvis C.R., Xiong Z.G., Plant J.R., Churchill D., Lu W.Y., MacVicar B.A., MacDonald J.F. Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons. J Neurophysiol. 78:1997;2363-2371.
31. Kang H., Schuman E.M. Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus. J Physiol Paris. 89:1995;11-22.
32. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1996;1658-1662.
33. Kang H., Welcher A.A., Shelton D., Schuman E.M. Neurotrophins and time different roles for TrkB signaling in hippocampal long-term potentiation . Neuron. 19:1997;653-664.
34. Kehoe P., Bronzino J.D. Neonatal stress alters LTP in freely moving male and female adult rats. Hippocampus. 9:1999;651-658.
35. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature. 386:1997;493-495.
36. Kempermann G., Kuhn H.G., Gage F.H. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA. 94:1997;10409-10414.
37. Kempermann G., Kuhn H.G., Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci. 18:1998;3206-3212.
38. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA. 92:1995;8856-8860.
39. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat age-related decrease of neuronal progenitor proliferation . J Neurosci. 16:1996;2027-2033.
40. Lauterborn J.C., Lynch G., Vanderklish P., Arai A., Gall C.M. Positive modulation of AMPA receptors increases neurotrophin expression by hippocampal and cortical neurons. J Neurosci. 20:2000;8-21.
41. Lee J., Duan W., Mattson M.P. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem. 82:2002;1367-1375.
42. Lemaire V., Koehl M., Le Moal M., Abrous D.N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA. 97:2000;11032-11037.
43. Lin S.Y., Wu K., Levine E.S., Mount H.T., Suen P.C., Black I.B. BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res Mol Brain Res. 55:1998;20-27.
44. McAllister A.K., Katz L.C., Lo D.C. Neurotrophins and synaptic plasticity. Annu Rev Neurosci. 22:1999;295-318.
45. McNaughton B.L., Barnes C.A. Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. J Comp Neurol. 175:1977;439-454.
46. Messaoudi E., Ying S.W., Kanhema T., Croll S.D., Bramham C.R. Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci. 22:2002;7453-7461.
47. Messaoudi E., Bardsen K., Srebro B., Bramham C.R. Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J Neurophysiol. 79:1998;496-499.
48. Neeper S.A., Gomez-Pinilla F., Choi J., Cotman C. Exercise and brain neurotrophins. Nature. 373:1995;109.
49. Nicoletti F., Valerio C., Pellegrino C., Drago F., Scapagnini U., Canonico P.L. Spatial learning potentiates the stimulation of phosphoinositide hydrolysis by excitatory amino acids in rat hippocampal slices. J Neurochem. 51:1988;725-729.
50. 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. Brain Res Mol Brain Res. 61:1998;147-153.
51. Orr G., Rao G., Houston F.P., McNaughton B.L., Barnes C.A. Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats. Hippocampus. 11:2001;647-654.
52. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron. 16:1996;1137-1145.
53. Pavlides C., Greenstein Y.J., Grudman M., Winson J. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res. 439:1988;383-387.
54. Rasmusson A.M., Shi L., Duman R. Downregulation of BDNF mRNA in the hippocampal dentate gyrus after re-exposure to cues previously associated with footshock. Neuropsychopharmacology. 27:2002;133-142.
55. Riedel G., Casabona G., Platt B., Macphail E.M., Nicoletti F. Fear conditioning-induced time- and subregion-specific increase in expression of mGlu5 receptor protein in rat hippocampus. Neuropharmacology. 39:2000;1943-1951.
56. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry. 7:2002;609-616.
57. Rosenzweig M.R., Bennett E.L. Psychobiology of plasticity effects of training and experience on brain and behavior . Behav Brain Res. 78:1996;57-65.
58. Russo-Neustadt A., Beard R.C., Cotman C.W. Exercise, antidepressant medications, and enhanced brain derived neurotrophic factor expression. Neuropsychopharmacology. 21:1999;679-682.
59. Russo-Neustadt A., Beard R.C., Huang Y.M., Cotman C.W. Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. J Neuroscience. 101:2001;305-312.
60. Schinder A.F., Poo M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23:2000;639-645.
61. Schuman E.M. mRNA trafficking and local protein synthesis at the synapse. Neuron. 23:1999;645-648.
62. Shors T.J., Dryver E. Effect of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus. Brain Res. 666:1994;232-238.
63. Shors T.J., Seib T.B., Levine S., Thompson R.F. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science. 244:1989;224-226.
64. Snyder J.S., Kee N., Wojtowicz J.M. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol. 85:2001;2423-2431.
65. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature. 401:1999;63-69.
66. Tang Y.P., Wang H., Feng R., Kyin M., Tsien J.Z. Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology. 41:2001;779-790.
67. Trejo J.L., Carro E., Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci. 21:2001;1628-1634.
68. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 2:1999;266-270.
69. van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA. 96:1999;13427-13431.
70. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., Gage F.H. Functional neurogenesis in the adult hippocampus. Nature. 415:2002;1030-1034.
71. Watabe A.M., O'Dell T.J. Age-related changes in theta frequency stimulation-induced long-term potentiation. Neurobiol Aging. 24:2003;267-272.
72. Ying S.W., Futter M., Rosenblum K., Webber M.J., Hunt S.P., Bliss T.V., Bramham C.R. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus requirement for ERK activation coupled to CREB and upregulation of Arc synthesis . J Neurosci. 22:2002;1532-1540.
73. Young D., Lawlor P.A., Leone P., Dragunow M., During M.J. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med. 5:1999;448-453.
74. Zhao X., Lein E.S., He A., Smith S.C., Aston C., Gage F.H. Transcriptional profiling reveals strict boundaries between hippocampal subregions. J Comp Neurol. 441:2000;187-196.