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Exercising Our Brains: How Physical Activity Impacts Synaptic Plasticity in the Dentate Gyrus

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Abstract

Exercise that engages the cardiovascular system has a myriad of effects on the body; however, we usually do not give much consideration to the benefits it may have for our minds. An increasing body of evidence suggests that exercise can have some remarkable effects on the brain. In this article, we will introduce how exercise can impact the capacity for neurons in the brain to communicate with one another. To properly convey this information, we will first briefly introduce the field of synaptic plasticity and then examine how the introduction of exercise to the experimental setting can actually alter the basic properties of synaptic plasticity in the brain. Next, we will examine some of the candidate physiological processes that might underlay these alterations. Finally, we will close by noting that, taken together, this data points toward our brains being dynamic systems that are in a continual state of flux and that physical exercise may help us to maximize the performance of both our body and our minds.

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References

  • Abraham, W. C., Logan, B., Greenwood, J. M., & Dragunow, M. (2002). Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. Journal of Neuroscience, 22, 9626–9634.

    PubMed  CAS  Google Scholar 

  • Adlard, P. A., & Cotman, C. W. (2004). Voluntary exercise protects against stress-induced decreases in brain-derived neurotrophic factor protein expression. Neuroscience, 124, 985–992.

    PubMed  CAS  Google Scholar 

  • Alfarez, D. N., Joels, M., & Krugers, H. J. (2003). Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. The European Journal of Neuroscience, 17, 1928–1934.

    PubMed  Google Scholar 

  • Avital, A., Segal, M., & Richter-Levin, G. (2006). Contrasting roles of corticosteroid receptors in hippocampal plasticity. Journal of Neuroscience, 26, 9130–9134.

    PubMed  CAS  Google Scholar 

  • Black, J. E., Isaacs, K. R., Anderson, B. J., Alcantara, A. A., & Greenough, W. T. (1990). Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proceedings of the National Academy of Sciences of the United States of America, 87, 5568–5572.

    PubMed  CAS  Google Scholar 

  • Bliss, T., Collingridge, G., & Morris, R. (2007). Synaptic Plasticity in the Hippocampus. In P. Andersen, R. Morris, D. Amaral, T. Bliss, & J. O'Keefe (Eds.), The hippocampus book (pp. 343–474). New York: Oxford University Press.

  • Bliss, T. V., & Gardner-Medwin, A. R. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. Journal of Physiology, 232, 357–374.

    PubMed  CAS  Google Scholar 

  • Bliss, T. V., & Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. Journal of Physiology, 232, 331–356.

    PubMed  CAS  Google Scholar 

  • Caldeira, M. V., Melo, C. V., Pereira, D. B., et al. (2007). Brain-derived neurotrophic factor regulates the expression and synaptic delivery of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons. Journal of Biological Chemistry, 282, 12619–12628.

    PubMed  CAS  Google Scholar 

  • Carro, E., Trejo, J. L., Busiguina, S., & Torres-Aleman, I. (2001). Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. Journal of Neuroscience, 21, 5678–5684.

    PubMed  CAS  Google Scholar 

  • Chao, H. M., Choo, P. H., & McEwen, B. S. (1989). Glucocorticoid and mineralocorticoid receptor mRNA expression in rat brain. Neuroendocrinology, 50, 365–371.

    PubMed  CAS  Google Scholar 

  • Chao, H. M., Sakai, R. R., Ma, L. Y., & McEwen, B. S. (1998). Adrenal steroid regulation of neurotrophic factor expression in the rat hippocampus. Endocrinology, 139, 3112–3118.

    PubMed  CAS  Google Scholar 

  • Chaudhury, D., Wang, L. M., & Colwell, C. S. (2005). Circadian regulation of hippocampal long-term potentiation. Journal of Biological Rhythms, 20, 225–236.

    PubMed  Google Scholar 

  • Chen, M. J., Ivy, A. S., & Russo-Neustadt, A. A. (2006). Nitric oxide synthesis is required for exercise-induced increases in hippocampal BDNF and phosphatidylinositol 3′ kinase expression. Brain Research Bulletin, 68, 257–268.

    PubMed  CAS  Google Scholar 

  • Christie, B. R., & Abraham, W. C. (1992a). Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron, 9, 79–84.

    PubMed  CAS  Google Scholar 

  • Christie, B. R., & Abraham, W. C. (1992b). NMDA-dependent heterosynaptic long-term depression in the dentate gyrus of anaesthetized rats. Synapse, 10, 1–6.

    PubMed  CAS  Google Scholar 

  • Christie, B. R., Kerr, D. S., & Abraham, W. C. (1994). Flip side of synaptic plasticity: Long-term depression mechanisms in the hippocampus. Hippocampus, 4, 127–135.

    PubMed  CAS  Google Scholar 

  • Christie, B. R., Swann, S. E., Fox, C. J., et al. (2005). Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. European Journal of Neuroscience, 21, 1719–1726.

    Article  PubMed  Google Scholar 

  • Claflin, D. I., Hennessy, M. B., & Jensen, S. J. (2005). Sex-specific effects of corticosterone on hippocampally mediated learning in young rats. Physiology & Behaviour, 85, 159–166.

    CAS  Google Scholar 

  • Conrad, C. D., Jackson, J. L., Wieczorek, L., et al. (2004). Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmacology, Biochemistry and Behavior, 78, 569–579.

    CAS  Google Scholar 

  • De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joels, M. (1998). Brain corticosteroid receptor balance in health and disease. Endocrine Reviews, 19, 269–301.

    PubMed  Google Scholar 

  • Dechant, G., & Barde, Y. A. (2002). The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nature Neuroscience, 5, 1131–1136.

    PubMed  CAS  Google Scholar 

  • Dey, S., Singh, R. H., & Dey, P. K. (1992). Exercise training: significance of regional alterations in serotonin metabolism of rat brain in relation to antidepressant effect of exercise. Physiology & Behaviour, 52, 1095–1099.

    CAS  Google Scholar 

  • Dougherty, K. D., & Milner, T. A. (1999). p75NTR immunoreactivity in the rat dentate gyrus is mostly within presynaptic profiles but is also found in some astrocytic and postsynaptic profiles. Journal of Comparative Neurology, 407, 77–91.

    PubMed  CAS  Google Scholar 

  • Douglas, R. M., & Goddard, G. V. (1975). Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus. Brain Research, 86, 205–215.

    PubMed  CAS  Google Scholar 

  • Droste, S. K., Gesing, A., Ulbricht, S., Muller, M. B., Linthorst, A. C., & Reul, J. M. (2003). Effects of long-term voluntary exercise on the mouse hypothalamic–pituitary–adrenocortical axis. Endocrinology, 144, 3012–3023.

    PubMed  CAS  Google Scholar 

  • Dudek, S. M., & Bear, M. F. (1992). Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proceedings of the National Academy of Sciences of the United States of America, 89, 4363–4367.

    PubMed  CAS  Google Scholar 

  • Dugich-Djordjevic, M. M., Tocco, G., Lapchak, P. A., et al. (1992). Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in the adult rat brain following seizures induced by systemic administration of kainic acid. Neuroscience, 47, 303–315.

    PubMed  CAS  Google Scholar 

  • Eadie, B. D., Redila, V. A., & Christie, B. R. (2005). Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. Journal of Comparative Neurology, 486, 39–47.

    PubMed  Google Scholar 

  • Engesser-Cesar, C., Ichiyama, R. M., Nefas, A. L., et al. (2007). Wheel running following spinal cord injury improves locomotor recovery and stimulates serotonergic fiber growth. European Journal of Neuroscience, 25, 1931–1939.

    PubMed  Google Scholar 

  • Farmer, J., Zhao, X., van Praag, H., Wodtke, K., Gage, F. H., & Christie, B. R. (2004). Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague–Dawley rats in vivo. Neuroscience, 124, 71–79.

    PubMed  CAS  Google Scholar 

  • Fediuc, S., Campbell, J. E., & Riddell, M. C. (2006). Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague–Dawley rats. Journal of Applied Physiology, 100, 1867–1875.

    PubMed  CAS  Google Scholar 

  • Ferreira, A., Chin, L. S., Li, L., Lanier, L. M., Kosik, K. S., & Greengard, P. (1998). Distinct roles of synapsin I and synapsin II during neuronal development. Molecular Medicine, 4, 22–28.

    PubMed  CAS  Google Scholar 

  • Figurov, A., Pozzo-Miller, L. D., Olafsson, P., Wang, T., & Lu, B. (1996). Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature, 381, 706–709.

    PubMed  CAS  Google Scholar 

  • Fox, C. J., Russell, K., Titterness, A. K., Wang, Y. T., & Christie, B. R. (2007). Tyrosine phosphorylation of the GluR2 subunit is required for long-term depression of synaptic efficacy in young animals in vivo. Hippocampus, 17, 600–605.

    PubMed  CAS  Google Scholar 

  • Foy, M. R., Stanton, M. E., Levine, S., & Thompson, R. F. (1987). Behavioral stress impairs long-term potentiation in rodent hippocampus. Behavioral and Neural Biology, 48, 138–149.

    PubMed  CAS  Google Scholar 

  • Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K., & Inokuchi, K. (2003). Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron, 38, 447–460.

    PubMed  CAS  Google Scholar 

  • Gerin, C., Legrand, A., & Privat, A. (1994). Study of 5-HT release with a chronically implanted microdialysis probe in the ventral horn of the spinal cord of unrestrained rats during exercise on a treadmill. Journal of Neuroscience Methods, 52, 129–141.

    PubMed  CAS  Google Scholar 

  • Glazner, G. W., & Mattson, M. P. (2000). Differential effects of BDNF, ADNF9, and TNFalpha on levels of NMDA receptor subunits, calcium homeostasis, and neuronal vulnerability to excitotoxicity. Experimental Neurology, 161, 442–452.

    PubMed  CAS  Google Scholar 

  • Gomez-Merino, D., Bequet, F., Berthelot, M., Chennaoui, M., & Guezennec, C. Y. (2001). Site-dependent effects of an acute intensive exercise on extracellular 5-HT and 5-HIAA levels in rat brain. Neuroscience Letters, 301, 143–146.

    PubMed  CAS  Google Scholar 

  • Gomez-Pinilla, F., Dao, L., & So, V. (1997). Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Research, 764, 1–8.

    PubMed  CAS  Google Scholar 

  • Hebb, C. O., & Konzett, H. (1949). The effect of certain analgesic drugs on synaptic transmission as observed in the perfused superior cervical ganglion of the cat. Quaterly Journal of Experimental Physiology and Cognate Medical Sciences, 35, 213–217.

    CAS  Google Scholar 

  • Herman, J. P., Patel, P. D., Akil, H., & Watson, S. J. (1989). Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Molecular Endocrinology, 3, 1886–1894.

    PubMed  CAS  Google Scholar 

  • Herman, J. P., Prewitt, C. M., & Cullinan, W. E. (1996). Neuronal circuit regulation of the hypothalamo–pituitary–adrenocortical stress axis. Critical Reviews in Neurobiology, 10, 371–394.

    PubMed  CAS  Google Scholar 

  • Hopper, R. A., & Garthwaite, J. (2006). Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. Journal of Neuroscience, 26, 11513–11521.

    PubMed  CAS  Google Scholar 

  • Ikegaya, Y., Ishizaka, Y., & Matsuki, N. (2002). BDNF attenuates hippocampal LTD via activation of phospholipase C: Implications for a vertical shift in the frequency-response curve of synaptic plasticity. European Journal of Neuroscience, 16, 145–148.

    PubMed  Google Scholar 

  • Isaacs, K. R., Anderson, B. J., Alcantara, A. A., Black, J. E., & Greenough, W. T. (1992). Exercise and the brain: Angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. Journal of Cerebral Blood Flow Metabolism, 12, 110–119.

    PubMed  CAS  Google Scholar 

  • Ivy, A. S., Rodriguez, F. G., Garcia, C., Chen, M. J., & Russo-Neustadt, A. A. (2003). Noradrenergic and serotonergic blockade inhibits BDNF mRNA activation following exercise and antidepressant. Pharmacology, Biochemistry and Behavior, 75, 81–88.

    CAS  Google Scholar 

  • Jacobsen, J. P., & Mork, A. (2006). Chronic corticosterone decreases brain-derived neurotrophic factor (BDNF) mRNA and protein in the hippocampus, but not in the frontal cortex, of the rat. Brain Research, 1110, 221–225.

    PubMed  CAS  Google Scholar 

  • Jacobson, L., & Sapolsky, R. (1991). The role of the hippocampus in feedback regulation of the hypothalamic–pituitary–adrenocortical axis. Endocrine Reviews, 12, 118–134.

    PubMed  CAS  Google Scholar 

  • Kim, J. J., Foy, M. R., & Thompson, R. F. (1996). Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proceedings of the National Academy of Sciences of the United States of America, 93, 4750–4753.

    PubMed  CAS  Google Scholar 

  • Kitraki, E., Kremmyda, O., Youlatos, D., Alexis, M. N., & Kittas, C. (2004). Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience, 125, 47–55.

    PubMed  CAS  Google Scholar 

  • Kohr, G., Jensen, V., Koester, H. J., et al. (2003). Intracellular domains of NMDA receptor subtypes are determinants for long-term potentiation induction. Journal of Neuroscience, 23, 10791–10799.

    PubMed  Google Scholar 

  • Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H., & Bonhoeffer, T. (1995). Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proceedings of the National Academy of Sciences of the United States of America, 92, 8856–8860.

    PubMed  CAS  Google Scholar 

  • Korte, M., Griesbeck, O., Gravel, C., et al. (1996). Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proceedings of the National Academy of Sciences of the United States of America, 93, 12547–12552.

    PubMed  CAS  Google Scholar 

  • Korz, V., & Frey, J. U. (2003). Stress-related modulation of hippocampal long-term potentiation in rats: Involvement of adrenal steroid receptors. Journal of Neuroscience, 23, 7281–7287.

    PubMed  CAS  Google Scholar 

  • Kovalchuk, Y., Hanse, E., Kafitz, K. W., & Konnerth, A. (2002). Postsynaptic induction of BDNF-mediated long-term potentiation. Science, 295, 1729–1734.

    PubMed  CAS  Google Scholar 

  • Kozorovitskiy, Y., & Gould, E. (2004). Dominance hierarchy influences adult neurogenesis in the dentate gyrus. Journal of Neuroscience, 24, 6755–6759.

    PubMed  CAS  Google Scholar 

  • Kramar, E. A., Lin, B., Rex, C. S., Gall, C. M., & Lynch, G. (2006). Integrin-driven actin polymerization consolidates long-term potentiation. Proceedings of the National Academy of Sciences of the United States of America, 103, 5579–5584.

    PubMed  CAS  Google Scholar 

  • Lahteinen, S., Pitkanen, A., Saarelainen, T., Nissinen, J., Koponen, E., & Castren, E. (2002). Decreased BDNF signalling in transgenic mice reduces epileptogenesis. European Journal of Neuroscience, 15, 721–734.

    PubMed  Google Scholar 

  • Larmet, Y., Reibel, S., Carnahan, J., Nawa, H., Marescaux, C., & Depaulis, A. (1995). Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. Neuroreport, 6, 1937–1941.

    PubMed  CAS  Google Scholar 

  • Lee, R., Kermani, P., Teng, K. K., & Hempstead, B. L. (2001). Regulation of cell survival by secreted proneurotrophins. Science, 294, 1945–1948.

    PubMed  CAS  Google Scholar 

  • Lee, H. K., Min, S. S., Gallagher, M., & Kirkwood, A. (2005). NMDA receptor-independent long-term depression correlates with successful aging in rats. Nature Neuroscience, 8, 1657–1659.

    PubMed  CAS  Google Scholar 

  • Lessmann, V., Gottmann, K., & Malcangio, M. (2003). Neurotrophin secretion: Current facts and future prospects. Progress in Neurobiology, 69, 341–374.

    PubMed  CAS  Google Scholar 

  • Lin, S. Y., Wu, K., Levine, E. S., Mount, H. T., Suen, P. C., & Black, I. B. (1998). BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Research. Molecular Brain Research, 55, 20–27.

    PubMed  CAS  Google Scholar 

  • Liu, L., Wong, T. P., Pozza, M. F., et al. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science, 304, 1021–1024.

    PubMed  CAS  Google Scholar 

  • Llorens-Martin, M., Torres-Aleman, I., & Trejo, J. L. (2006). Pronounced individual variation in the response to the stimulatory action of exercise on immature hippocampal neurons. Hippocampus, 16, 480–490.

    PubMed  CAS  Google Scholar 

  • Malek, Z. S., Sage, D., Pevet, P., & Raison, S. (2007). Daily rhythm of tryptophan hydroxylase-2 messenger ribonucleic acid within raphe neurons is induced by corticoid daily surge and modulated by enhanced locomotor activity. Endocrinology, 148, 5165–5172.

    PubMed  CAS  Google Scholar 

  • Marin, H., & Menza, M. A. (2005). The management of fatigue in depressed patients. Essential Psychopharmacology, 6, 185–192.

    PubMed  Google Scholar 

  • Mattson, M. P., Maudsley, S., & Martin, B. (2004). BDNF and 5-HT: A dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends in Neurosciences, 27, 589–594.

    PubMed  CAS  Google Scholar 

  • McCloskey, D. P., Adamo, D. S., & Anderson, B. J. (2001). Exercise increases metabolic capacity in the motor cortex and striatum, but not in the hippocampus. Brain Research, 891, 168–175.

    PubMed  CAS  Google Scholar 

  • McNaughton, B. L., Douglas, R. M., & Goddard, G. V. (1978). Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents. Brain Research, 157, 277–293.

    PubMed  CAS  Google Scholar 

  • Meeusen, R., Thorre, K., Chaouloff, F., et al. (1996). Effects of tryptophan and/or acute running on extracellular 5-HT and 5-HIAA levels in the hippocampus of food-deprived rats. Brain Research, 740, 245–252.

    PubMed  CAS  Google Scholar 

  • Mowla, S. J., Farhadi, H. F., Pareek, S., et al. (2001). Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. Journal of Biological Chemistry, 276, 12660–12666.

    PubMed  CAS  Google Scholar 

  • Mowla, S. J., Pareek, S., Farhadi, H. F., et al. (1999). Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons. Journal of Neuroscience, 19, 2069–2080.

    PubMed  CAS  Google Scholar 

  • Neeper, S. A., Gomez-Pinilla, F., Choi, J., & Cotman, C. (1995). Exercise and brain neurotrophins. Nature, 373, 109.

    PubMed  CAS  Google Scholar 

  • Neeper, S. A., Gomez-Pinilla, F., Choi, J., & Cotman, C. W. (1996). Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Research, 726, 49–56.

    PubMed  CAS  Google Scholar 

  • Oberlander, T. F., Warburton, W., Misri, S., Aghajanian, J., & Hertzman, C. (2006). Neonatal outcomes after prenatal exposure to selective serotonin reuptake inhibitor antidepressants and maternal depression using population-based linked health data. Archives of General Psychiatry, 63, 898–906.

    PubMed  Google Scholar 

  • Owens, M. J. (2004). Selectivity of antidepressants: From the monoamine hypothesis of depression to the SSRI revolution and beyond. Journal of Clinical Psychiatry, 65(Suppl 4), 5–10.

    PubMed  CAS  Google Scholar 

  • Patterson, S. L., Abel, T., Deuel, T. A., Martin, K. C., Rose, J. C., & Kandel, E. R. (1996). Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron, 16, 1137–1145.

    PubMed  CAS  Google Scholar 

  • Pavlides, C., Ogawa, S., Kimura, A., & McEwen, B. S. (1996). Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices. Brain Research, 738, 229–235.

    PubMed  CAS  Google Scholar 

  • Peris, J., Anderson, K. J., Vickroy, T. W., King, M. A., Hunter, B. E., & Walker, D. W. (1997). Neurochemical basis of disruption of hippocampal long-term potentiation by chronic alcohol exposure. Frontiers in Bioscience, 2, d309–d316.

    PubMed  CAS  Google Scholar 

  • Pozzo-Miller, L. D., Gottschalk, W., Zhang, L., et al. (1999). Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. Journal of Neuroscience, 19, 4972–4983.

    PubMed  CAS  Google Scholar 

  • Radecki, D. T., Brown, L. M., Martinez, J., & Teyler, T. J. (2005). BDNF protects against stress-induced impairments in spatial learning and memory and LTP. Hippocampus, 15, 246–253.

    PubMed  CAS  Google Scholar 

  • Redila, V. A., & Christie, B. R. (2006). Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience, 137, 1299–1307.

    PubMed  CAS  Google Scholar 

  • Reibel, S., Larmet, Y., Le, B. T., Carnahan, J., Marescaux, C., & Depaulis, A. (2000). Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience, 100, 777–788.

    PubMed  CAS  Google Scholar 

  • Remondes, M., & Schuman, E. M. (2004). Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature, 431, 699–703.

    PubMed  CAS  Google Scholar 

  • Rex, C. S., Lin, C. Y., Kramar, E. A., Chen, L. Y., Gall, C. M., & Lynch, G. (2007). Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. Journal of Neuroscience, 27, 3017–3029.

    PubMed  CAS  Google Scholar 

  • Schaaf, M. J., de Jong, J., de Kloet, E. R., & Vreugdenhil, E. (1998). Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Research, 813, 112–120.

    PubMed  CAS  Google Scholar 

  • Schaaf, M. J., Duurland, R., de Kloet, E. R., & Vreugdenhil, E. (2000). Circadian variation in BDNF mRNA expression in the rat hippocampus. Brain Research. Molecular Brain Research, 75, 342–344.

    PubMed  CAS  Google Scholar 

  • Schaaf, M. J., Hoetelmans, R. W., de Kloet, E. R., & Vreugdenhil, E. (1997). Corticosterone regulates expression of BDNF and TrkB but not NT-3 and TrkC mRNA in the rat hippocampus. Journal of Neuroscience Research, 48, 334–341.

    PubMed  CAS  Google Scholar 

  • Shors, T. J., & Thompson, R. F. (1992). Acute stress impairs (or induces) synaptic long-term potentiation (LTP) but does not affect paired-pulse facilitation in the stratum radiatum of rat hippocampus. Synapse, 11, 262–265.

    PubMed  CAS  Google Scholar 

  • Sjosten, N., & Kivela, S. L. (2006). The effects of physical exercise on depressive symptoms among the aged: A systematic review. International Journal of Geriatric Psychiatry, 21, 410–418.

    PubMed  Google Scholar 

  • Smith, M. A., Makino, S., Kvetnansky, R., & Post, R. M. (1995). Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. Journal of Neuroscience, 15, 1768–1777.

    PubMed  CAS  Google Scholar 

  • Spencer, R. L., Kim, P. J., Kalman, B. A., & Cole, M. A. (1998). Evidence for mineralocorticoid receptor facilitation of glucocorticoid receptor-dependent regulation of hypothalamic–pituitary–adrenal axis activity. Endocrinology, 139, 2718–2726.

    PubMed  CAS  Google Scholar 

  • Spier, S. A., Delp, M. D., Meininger, C. J., Donato, A. J., Ramsey, M. W., & Muller-Delp, J. M. (2004). Effects of ageing and exercise training on endothelium-dependent vasodilatation and structure of rat skeletal muscle arterioles. Journal of Physiology, 556, 947–958.

    PubMed  CAS  Google Scholar 

  • Stranahan, A. M., Khalil, D., & Gould, E. (2007). Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus, 17, 1017–1022.

    PubMed  Google Scholar 

  • Struder, H. K., & Weicker, H. (2001). Physiology and pathophysiology of the serotonergic system and its implications on mental and physical performance. Part II. International Journal of Sports Medicine, 22, 482–497.

    PubMed  CAS  Google Scholar 

  • Stummer, W., Weber, K., Tranmer, B., Baethmann, A., & Kempski, O. (1994). Reduced mortality and brain damage after locomotor activity in gerbil forebrain ischemia. Stroke, 25, 1862–1869.

    PubMed  CAS  Google Scholar 

  • Swain, R. A., Harris, A. B., Wiener, E. C., et al. (2003). Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience, 117, 1037–1046.

    PubMed  CAS  Google Scholar 

  • Thiele, C., Hannah, M. J., Fahrenholz, F., & Huttner, W. B. (2000). Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nature Cell Biology, 2, 42–49.

    PubMed  CAS  Google Scholar 

  • Thinschmidt, J. S., Walker, D. W., & King, M. A. (2003). Chronic ethanol treatment reduces the magnitude of hippocampal LTD in the adult rat. Synapse, 48, 189–197.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Tyler, W. J., & Pozzo-Miller, L. D. (2001). BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. Journal of Neuroscience, 21, 4249–4258.

    PubMed  CAS  Google Scholar 

  • Van Eekelen, J. A., & De Kloet, E. R. (1992). Co-localization of brain corticosteroid receptors in the rat hippocampus. Progress in Histochemistry and Cytochemistry, 26, 250–258.

    PubMed  Google Scholar 

  • Van Eekelen, J. A., Jiang, W., De Kloet, E. R., & Bohn, M. C. (1988). Distribution of the mineralocorticoid and the glucocorticoid receptor mRNAs in the rat hippocampus. Journal of Neuroscience Research, 21, 88–94.

    PubMed  Google Scholar 

  • 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 of the United States of America, 96, 13427–13431.

    PubMed  Google Scholar 

  • van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature, 415, 1030–1034.

    PubMed  Google Scholar 

  • van Praag, H., Shubert, T., Zhao, C., & Gage, F. H. (2005). Exercise enhances learning and hippocampal neurogenesis in aged mice. Journal of Neuroscience, 25, 8680–8685.

    PubMed  Google Scholar 

  • Vasuta, C., Caunt, C., & James, R., et al. (2007). Effects of exercise on NMDA receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus. Hippocampus, 17, 1201–1208.

    PubMed  CAS  Google Scholar 

  • Vaynman, S. S., Ying, Z., Yin, D., & Gomez-Pinilla, F. (2006). Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Research, 1070, 124–130.

    PubMed  CAS  Google Scholar 

  • Wadley, V. G., McClure, L. A., Howard, V. J., et al. (2007). Cognitive status, stroke symptom reports, and modifiable risk factors among individuals with no diagnosis of stroke or transient ischemic attack in the reasons for geographic and racial differences in stroke (REGARDS) study. Stroke, 38, 1143–1147.

    PubMed  Google Scholar 

  • Wilson, W. M., & Marsden, C. A. (1996). In vivo measurement of extracellular serotonin in the ventral hippocampus during treadmill running. Behavioural Pharmacology, 7, 101–104.

    PubMed  CAS  Google Scholar 

  • Woo, N. H., Teng, H. K., Siao, C. J., et al. (2005). Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nature Neuroscience, 8, 1069–1077.

    PubMed  CAS  Google Scholar 

  • Xiong, W., Wei, H., Xiang, X., et al. (2004). The effect of acute stress on LTP and LTD induction in the hippocampal CA1 region of anesthetized rats at three different ages. Brain Research, 1005, 187–192.

    PubMed  CAS  Google Scholar 

  • Wu, K., Xu, J. L., Suen, P. C., et al. (1996). Functional TrkB neurotrophin receptors are intrinsic components of the adult brain postsynaptic density. Brain Research. Molecular Brain Research, 43, 286–290.

    PubMed  CAS  Google Scholar 

  • Xiong, W., Yang, Y., Cao, J., et al. (2003). The stress experience dependent long-term depression disassociated with stress effect on spatial memory task. Neuroscience Research, 46, 415–421.

    PubMed  Google Scholar 

  • Xu, L., Anwyl, R., & Rowan, M. J. (1997). Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature, 387, 497–500.

    PubMed  CAS  Google Scholar 

  • Xu, L., Holscher, C., Anwyl, R., & Rowan, M. J. (1998). Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proceedings of the National Academy of Sciences of the United States of America, 95, 3204–3208.

    PubMed  CAS  Google Scholar 

  • Xu, B., Michalski, B., Racine, R. J., & Fahnestock, M. (2004). The effects of brain-derived neurotrophic factor (BDNF) administration on kindling induction, Trk expression and seizure-related morphological changes. Neuroscience, 126, 521–531.

    PubMed  CAS  Google Scholar 

  • Yancey, S. L., & Overton, J. M. (1993). Cardiovascular responses to voluntary and treadmill exercise in rats. Journal of Applied Physiology, 75, 1334–1340.

    PubMed  CAS  Google Scholar 

  • Zhou, J., Zhang, F., & Zhang, Y. (2000). Corticosterone inhibits generation of long-term potentiation in rat hippocampal slice: Involvement of brain-derived neurotrophic factor. Brain Research, 885, 182–191.

    PubMed  CAS  Google Scholar 

  • Zhu, W. J., & Roper, S. N. (2001). Brain-derived neurotrophic factor enhances fast excitatory synaptic transmission in human epileptic dentate gyrus. Annals of Neurology, 50, 188–194.

    PubMed  CAS  Google Scholar 

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Acknowledgments

This work was funded by grants from NSERC, CIHR, and ABMRF to BRC. BRC is a Michael Smith Foundation Senior Scholar. BDE is a CIHR graduate scholarship recipient. JS is a UVIC graduate scholarship recipient. AKT holds a University Graduate Fellowship, a Pacifica Family Addiction Foundation Geoffrey Lane Nanson Scholarship and The Pacific Century Graduate Scholarship at UBC.

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  1. Division of Medical Sciences and Department of Biology, University of Victoria, P.O. Box 1700, STN CSC, Victoria, BC, Canada, V8W 2Y2

    Brian R. Christie, Brennan D. Eadie, Timal S. Kannangara, Julie M. Robillard, James Shin & Andrea K. Titterness

  2. Neuroscience Program, The Brain Research Centre, Department of Cellular and Physiological Sciences, University of British Columbia, Vancouver, BC, Canada

    Brian R. Christie, Brennan D. Eadie, Timal S. Kannangara, Julie M. Robillard, James Shin & Andrea K. Titterness

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  1. Brian R. Christie
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  2. Brennan D. Eadie
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Correspondence to Brian R. Christie.

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Christie, B.R., Eadie, B.D., Kannangara, T.S. et al. Exercising Our Brains: How Physical Activity Impacts Synaptic Plasticity in the Dentate Gyrus. Neuromol Med 10, 47–58 (2008). https://doi.org/10.1007/s12017-008-8033-2

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