Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running

Behavioral Neuroscience

Volumn 117, Issue 5, 2003, Pages 1006-1016

  Rhodes, Justin S ^a,e   Jeffrey, Susan ^c   Girard, Isabelle ^a   Mitchell, Gordon S ^c   Van Praag, Henriette ^b   Garland Jr , Theodore ^d   Gage, Fred H ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL DIVISION; CELL LABELING; CONTROLLED STUDY; CORRELATION ANALYSIS; DEPTH PERCEPTION; EXERCISE; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING; LOCOMOTION; MAZE TEST; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; RUNNING; SPATIAL MEMORY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; BREEDING; CELL COUNT; EXERTION; FEMALE; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, INBRED ICR; MOTOR ACTIVITY; NEURONS;

EID: 0141919620     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.117.5.1006     Document Type: Article

References (83)

1. Allen, D. M., van Praag, H., Ray, J., Weaver, Z., Winrow, C. J., Carter, T. A., et al. (2001). Ataxia telangiectasia mutated is essential during adult neurogenesis. Genes and Development, 15, 554-566.
2. Anderson, B. J., Rapp, D. N., Baek, D. H., McCloskey, D. P., Coburn-Litvak, P. S., & Robinson, J. K. (2000). Exercise influences spatial learning in the radial arm maze. Physiology & Behavior. 70, 425-429.
3. Arvidsson, A., Kokaia, Z., & Lindvall, O. (2001). N-methyl-D-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. European Journal of Neuroscience, 14, 10-18.
4. Bardgett, M. E., & Henry, J. D. (1999). Locomotor activity and accumbens Fos expression driven by ventral hippocampal stimulation require DI and D2 receptors. Neuroscience, 94, 59-70.
5. Biebl, M., Cooper, C. M., Winkler, J., & Kuhn, H. G. (2000). Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neuroscience Letters, 291, 17-20.
6. Biegler, R., McGregor, A., Krebs, J. R., & Healy, S. D. (2001). A larger hippocampus is associated with longer-lasting spatial memory. Proceedings of the National Academy of Sciences, USA, 98, 6941-6944.
7. Black, I. B. (1999). Trophic regulation of synaptic plasticity. Journal of Neurobiology, 41, 108-118.
8. Boyes, B. E., Kim, S. U., Lee, V., & Sung, S. C. (1986). Immunohistochemical co-localization of S-100β and the glial fibrillary acidic protein in rat brain. Neuroscience, 17, 857-865.
9. Brudzynski, S. M., & Gibson, C. J. (1997). Release of dopamine in the nucleus accumbens caused by stimulation of the subiculum in freely moving rats. Brain Research Bulletin, 42, 303-308.
10. Carro, E., Nunez, A., Busiguina, S., & Torres-Aleman, I. (2000). Circulating insulin-like growth factor I mediates effects of exercise on the brain. Journal of Neuroscience, 20, 2926-2933.
11. Deweer, B., Pillon, B., Pochon, J. B., & Dubois, B. (2001). Is the HM story only a "remote memory"? Some facts about hippocampus and memory in humans. Behavioural Brain Research, 127, 209-224.
12. Dohm, M. R., Richardson, C. S., & Garland, T., Jr. (1994). Exercise physiology of wild and random-bred laboratory house mice and their reciprocal hybrids. American Journal of Physiology, 267, R1098-R1108.
13. Feng, R., Rampon, C., Tang, Y. P., Shrom, D., Jin, J., Kyin, M., et al. (2001). Deficient neurogenesis in forebrain-specific presenilin-1 knock-out mice is associated with reduced clearance of hippocampal memory traces. Neuron, 32, 911-926.
14. Floresco, S. B., Todd, C. L., & Grace, A. A. (2001). Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. Journal of Neuroscience, 21, 4915-4922.
15. Fordyce, D. E., & Farrar, R. P. (1991). Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behavioural Brain Research, 46, 123-133.
16. Fordyce, D. E., & Wehner, J. M. (1993). Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase C activity in C57BL/6 and DBA/2 mice. Brain Research, 619, 111-119.
17. Fortin, N. J., Agster, K. L., & Eichenbaum, H. B. (2002). Critical role of the hippocampus in memory for sequences of events. Nature Neuroscience, 5, 458-462.
18. Gage, F. H. (2000, February 25). Mammalian neural stem cells. Science, 287, 1433-1438.
19. Gage, F. H., Kempermann, G., Palmer, T. D., Peterson, D. A., & Ray, J. (1998). Multipotent progenitor cells in the adult dentate gyrus. Journal of Neurobiology, 36, 249-266.
20. Garland, T., Jr. (2003). Selection experiments: An underutilized tool in biomechanics and organismal biology. In V. Bels, J. Gasc, & A. Casinos (Eds.), Biomechanics and evolution (pp. 23-56). Oxford, England: Bios Scientific Publishers.
21. Gerlai, R. T., McNamara, A., Williams, S., & Phillips, H. S. (2002). Hippocampal dysfunction and behavioral deficit in the water maze in mice: An unresolved issue? Brain Research Bulletin, 57, 3-9.
22. Girard, I., & Garland, T., Jr. (2002). Plasma corticosterone response to acute and chronic voluntary exercise in female house mice. Journal of Applied Physiology, 92, 1553-1561.
23. Girard, I., McAleer, M. W., Rhodes, J. S., & Garland, T., Jr. (2001). Selection for high voluntary wheel-running increases speed and intermittency in house mice (Mus domesticus). Journal of Experimental Biology, 204, 4311-4320.
24. Gomez-Pinilla, F., So, V., & Kesslak, J. P. (1998). Spatial learning and physical activity contribute to the induction of fibroblast growth factor: Neural substrates for increased cognition associated with exercise. Neuroscience, 85, 53-61.
25. Gould, E. (1994). The effects of adrenal steroids and excitatory input on neuronal birth and survival. In V. N. Luine & C. F. Harding (Eds.), Annals of the New York Academy of Sciences: Vol. 743. Hormonal restructuring of the adult brain: Basic and clinical perspectives (pp. 73-92). New York: New York Academy of Sciences.
26. Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nature Neuroscience, 2, 260-265.
27. Gould, E., Reeves, A. J., Graziano, M. S., & Gross, C. G. (1999, October 15). Neurogenesis in the neocortex of adult primates. Science, 286, 548-552.
28. Henderson, N. (1989). Interpreting studies that compare high- and low-selected lines on new characters. Behavior Genetics, 19, 473-502.
29. Henderson, N. (1997). Spurious association in unreplicated selected lines. Behavior Genetics, 27, 145-154.
30. Jacobs, B. L., van Praag, H., & Gage, F. H. (2000). Adult brain neurogenesis and psychiatry: A novel theory of depression. Molecular Psychiatry, 5, 262-269.
31. Jin, K., Minami, M., Lan, J. Q., Mao, X. O., Batteur, S., Simon, R. P., & Greenberg, D. A. (2001). Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proceedings of the National Academy of Sciences, USA, 98, 4710-4715.
32. Johnson, R. A., Rhodes, J. S., Jeffrey, S. L., Garland, T., Jr., & Mitchell, G. S. (in press). Hippocampal brain-derived neurotrophic factor but not nuerotrophin-3 increases more in mice selected for increase voluntary wheel running. Neuroscience.
33. Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997a). Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proceedings of the National Academy of Sciences, USA, 94, 10409-10414.
34. Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997b, April 3). More hippocampal neurons in adult mice living in an enriched environment. Nature, 386, 493-495.
35. Kuhn, H. G., Dickinson-Anson, H., & Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. Journal of Neuroscience, 16, 2027-2033.
36. Lavenex, P. B., Lavenex, P., & Clayton, N. S. (2001). Comparative studies of postnatal neurogenesis and learning: A critical review. Avian and Poultry Biology Reviews, 12, 103-125.
37. Lee, J., Duan, W., Long, J. M., Ingram, D. K., & Mattson, M. P. (2000). Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats. Journal of Molecular Neuroscience, 15, 99-108.
38. Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proceedings of the National Academy of Sciences, USA, 97, 11032-11037.
39. Li, X. C., Jarvis, E. D., Alvarez-Borda, B., Lim, D. A., & Nottebohm, F. (2000). A relationship between behavior, neurotrophin expression, and new neuron survival. Proceedings of the National Academy of Sciences, USA, 97, 8584-8589.
40. Littell, R. C., Milliken, G. A., Stroup, W. W., & Wolfinger, R. D. (1996). SAS system for mixed models. Cary, NC: SAS Institute.
41. Malberg, J. E., Eisch, A. J., Nestler, E. J., & Duman, R. S. (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. Journal of Neuroscience, 20, 9104-9110.
42. McFarland, W. L., Teitelbaum, H., & Hedges, E. K. (1975). Relationship between hippocampal theta activity and running speed in the rat. Journal of Comparative Physiology and Psychology, 88, 324-328.
43. McNaughton, B. L., Barnes, C. A., & O'Keefe, J. (1983). The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Experimental Brain Research, 52, 41-49.
44. Meeusen, R., Smolders, I., Sarre, S., de Meirleir, K., Keizer, H., Serneels, M., et al. (1997). Endurance training effects on neurotransmitter release in rat striatum: An in vivo microdialysis study. Acta Physiologica Scandinavia, 159, 335-341.
45. Morris, R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods, 11, 47-60.
46. Morris, R., & Hagan, J. J. (1983). Hippocampal electrical activity and ballistic movement. In W. Seifert (Ed.), Neurobiology of the hippocampus (pp. 321-331). London: Academic Press.
47. Mullen, R. J., Buck, C. R., & Smith, A. M. (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116, 201-211.
48. Myhrer, T. (1975). Normal jump avoidance performance in rats with the hippocampal theta rhythm selectively disrupted. Behavioral Biology, 14, 489-498.
49. Nanda, S. A., & Mack, K. J. (2000). Seizures and sensory stimulation result in different patterns of brain derived neurotrophic factor protein expression in the barrel cortex and hippocampus. Molecular Brain Research, 78, 1-14.
50. Neeper, S. A., Gomez-Pinilla, F., Choi, J., & Cotman, C. (1995, January 12). Exercise and brain neurotrophins. Nature, 373, 109.
51. Oddie, S. D., & Bland, B. H. (1998). Hippocampal formation theta activity and movement selection. Neuroscience and Biobehavioral Reviews, 22, 221-231.
52. Okragly, A. J., & Haak-Frendscho, M. (1997). An acid-treatment method for the enhanced detection of GDNF in biological samples. Experimental Neurology, 145, 592-596.
53. Oladehin, A., & Waters, R. S. (2001). Location and distribution of Fos protein expression in rat hippocampus following acute moderate aerobic exercise. Experimental Brain Research, 137, 26-35.
54. Oliff, H. S., Berchtold, N. C., Isackson, P., & Cotman, C. W. (1998). Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus. Molecular Brain Research, 61, 147-153.
55. Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., & Lowenstein, D. H. (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. Journal of Neuroscience, 17, 3727-3738.
56. Patterson, S. L., Grover, L. M., Schwartzkroin, P. A., & Bothwell, M. (1992). Neurotrophin expression in rat hippocampal slices: A stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron, 9, 1081-1088.
57. Pencea, V., Bingaman, K. D., Wiegand, S. J., & Luskin, M. B. (2001). Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. Journal of Neuroscience, 21, 6706-6717.
58. Pinheiro, J. C., & Bates, D. M. (2000). Mixed-effects models in S and S-Plus. New York: Springer.
59. Ploeger, G. E., Spruijt, B. M., & Cools, A. R. (1994). Spatial localization in the Morris water maze in rats: Acquisition is affected by intra-accumbens injections of the dopaminergic antagonist haloperidol. Behavioral Neuroscience, 108, 927-934.
60. Rakic, P. (2002). Adult neurogenesis in mammals: An identity crisis. Journal of Neuroscience, 22, 614-618.
61. Rhodes, J. S., & Garland, T., Jr. (2003). Differential sensitivity to acute administration of Ritalin, apomporphine, SCH 23390, but not raclopride in mice selectively bred for hyperactive wheel-running behavior. Psychopharmacology, 167, 242-250.
62. Rhodes, J. S., Garland, T., Jr., & Gammie, S. C. (in press). Patterns of brain activity associated with variation in voluntary wheel-running behavior. Behavioral Neuroscience.
63. Rhodes, J. S., Hosack, G. R., Girard, I., Kelley, A. E., Mitchell, G. S., & Garland, T., Jr. (2001). Differential sensitivity to acute administration of cocaine, GBR 12909, and fluoxetine in mice selectively bred for hyperactive wheel-running behavior. Psychopharmacology, 158, 120-131.
64. Sapolsky, R. M. (1996, August 9). Why stress is bad for your brain. Science, 273, 749-750.
65. Sforzo, G. A., Seeger, T. F., Pert, C. B., Pert, A., & Dotson, C. O. (1986). In vivo opioid receptor occupation in the rat brain following exercise. Medicine and Science in Sports and Exercise, 18, 380-384.
66. Slawinska, U., & Kasicki, S. (1998). The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion. Brain Research, 796, 327-331.
67. Suzuki, W. A., & Clayton, N. S. (2000). The hippocampus and memory: A comparative and ethological perspective. Current Opinions in Neurobiology, 10, 769-773.
68. Swallow, J. G., Carter, P. A., & Garland, T., Jr. (1998). Artificial selection for increased wheel-running behavior in house mice. Behavior Genetics, 28, 227-237.
69. Swallow, J. G., Koteja, P., Carter, P. A., & Garland, T. (1999). Artificial selection for increased wheel-running activity in house mice results in decreased body mass at maturity. Journal of Experimental Biology, 202, 2513-2520.
70. Swanson, L. W. (1983). The hippocampus and the concept of the limbic system. In W. Seifert (Ed.), Neurobiology of the hippocampus (pp. 3-19). London: Academic Press.
71. Tracy, A. L., Jarrard, L. E., & Davidson, T. L. (2001). The hippocampus and motivation revisited: Appetite and activity. Behavioural Brain Research, 127, 13-23.
72. Trejo, J. L., Carro, E., & Torres-Aleman, I. (2001). Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. Journal of Neuroscience, 21, 1628-1634.
73. Vanderwolf, C. H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalography and Clinical Neurophysiology, 26, 407-418.
74. van Praag, H., Christie, B. R., Sejnowski, T. J., & Gage, F. H. (1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences, USA, 96, 13427-13431.
75. van Praag, H., Kempermann, G., & Gage, F. H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience, 2, 266-270.
76. van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002, February 28). Functional neurogenesis in the adult hippocampus. Nature, 415, 1030-1034.
77. Warren, S. G., & Juraska, J. M. (1997). Spatial and nonspatial learning across the rat estrous cycle. Behavioral Neuroscience, 111, 259-266.
78. West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991). Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. The Anatomical Record, 231, 482-497.
79. Widenfalk, J., Olson, L., & Thoren, P. (1999). Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain. Neuroscience Research, 34, 125-132.
80. Wittenberg, G. M., & Tsien, J. Z. (2002). An emerging molecular and cellular framework for memory processing by the hippocampus. Trends in Neuroscience, 25, 501-505.
81. Wu, M., & Brudzynski, S. M. (1995). Mesolimbic dopamine terminals and locomotor activity induced from the subiculum. NeuroReport, 6, 1601-1604.
82. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H., & Lindholm, D. (1990). Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO Journal, 9, 3545-3550.
83. Zuo, M. X. (1998). The studies on neurogenesis induced by brain injury in adult ring dove. Cell Research, 8, 151-158.