All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis

Vivar, Carmen; Potter, Michelle C.; van Praag, Henriette

doi:10.1007/7854_2012_220

Cited by 370Neurogenesis and neuroplasticity mechanismsMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis

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Vivar, Carmen, Potter, Michelle C., van Praag, Henriette·2012·Current Topics in Behavioral Neurosciences

DOI 10.1007/7854_2012_220PMC PMC4565722

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Abstract

Accumulating evidence from animal and human research shows exercise benefits learning and memory, which may reduce the risk of neurodegenerative diseases, and could delay age-related cognitive decline. Exercise-induced improvements in learning and memory are correlated with enhanced adult hippocampal neurogenesis and increased activity-dependent synaptic plasticity. In this present chapter we will highlight the effects of physical activity on cognition in rodents, as well as on dentate gyrus (DG) neurogenesis, synaptic plasticity, spine density, neurotransmission and growth factors, in particular brain-derived nerve growth factor (BDNF).

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Physical exercise activates adult neurogenesis in the dentate gyrus of the hippocampus.
“Voluntary physical exercise is also a very effective inducer of adult neurogenesis in the dentate gyrus (van Praag et al., 1999a, b;Vivar et al., 2013).”
From Depression and adult neurogenesis: Positive effects of the antidepressant fluoxetine and of physical exercise (2018) · cites this paper as Vivar et al., 2013
Physical exercise improves performance on hippocampus-dependent cognitive tasks and reduces anxiety-like behaviors.
“Indeed, numerous studies have shown that physical exercise improves performance on hippocampus-dependent cognitive tasks (reviewed in Vivar et al., 2013) and reduces anxiety-like behaviors (Schoenfeld et al., 2013).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Vivar et al., 2013
Aerobic exercise is thought to enhance synaptic efficiency through promoting synaptic plasticity, such as through facilitating long-term potentiation.
“Learning and memory is reliant upon the efficient communication between neural cells through their synapses and AE is thought to enhance this efficiency through promoting synaptic plasticity in a number of ways (Vivar et al., 2013), such as through facilitating long-term potentiation (LTP).”
From Aerobic Exercise as a Tool to Improve Hippocampal Plasticity and Function in Humans: Practical Implications for Mental Health Treatment (2016) · cites this paper as Vivar et al., 2013
Exercise incorporating goal-based motor skill learning improves motor skill performance in PD, and this may be enhanced through cognitive engagement.
“The general idea is that exercise incorporating goal based motor skill learning improves motor skill performance in PD and that this may be enhanced through cognitive engagement.”
From Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease (2013) · cites this paper as [125]

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Background
Context Fear Learning in the Absence of the Hippocampus
Wiltgen, B. J., Sanders, M. J., Anagnostaras, S., Sage, J. R., & Fanselow, M. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2685-05.2006 · Cited by 349 · see citing works
Behavioral functions of the CA3 subregion of the hippocampusPreprint
Kesner, R. P. (2007) · Learning & Memory · doi:10.1101/lm.688207 · Cited by 337 · see citing works
Subsynaptic Plate Perforations: Changes with Age and Experience in the Rat
Greenough, W. T., West, R. W., & DeVoogd, T. J. (1978) · Science · doi:10.1126/science.715459 · Cited by 330 · see citing works
Running induces widespread structural alterations in the hippocampus and entorhinal cortex
Stranahan, A. M., Khalil, D., & Gould, E. (2007) · Hippocampus · doi:10.1002/hipo.20348 · Cited by 327 · see citing works
Antidepressant effects of exercise: Evidence for an adult-neurogenesis hypothesis?
Ernst, C., Olson, A. K., Pinel, J. P. J., Lam, R. W., & Christie, B. R. (2006) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0610 · Cited by 322 · see citing works
Physical exercise and brain monoamines: a review.
CHAOULOFF, F. (1989) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1989.tb08715.x · Cited by 316 · see citing works
Running throughout middle-age improves memory function, hippocampal neurogenesis, and BDNF levels in female C57BL/6J mice
Marlatt, M. W., Potter, M. C., Lucassen, P. J., & van Praag, H. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22009 · Cited by 314 · see citing works
Self-citation
Regional Effects of Wheel Running and Environmental Enrichment on Cell Genesis and Microglia Proliferation in the Adult Murine Neocortex
Ehninger, D. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.8.845 · Cited by 314 · see citing works
Plant-Derived Flavanol (−)Epicatechin Enhances Angiogenesis and Retention of Spatial Memory in Mice
van Praag, H., Lucero, M. J., Yeo, G. W., Stecker, K., Heivand, N., Zhao, C., Yip, E., Afanador, M., Schroeter, H., Hammerstone, J., et al. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0914-07.2007 · Cited by 303 · see citing works
Self-citation
Depression, Antidepressants, and Neurogenesis: A Critical Reappraisal
Hanson, N. D., Owens, M. J., & Nemeroff, C. B. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.220 · Cited by 302 · see citing works
Physical exercise induces FGF-2 and its mRNA in the hippocampus
Gómez‐Pinilla, F., Dao, L., & So, V. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00375-2 · Cited by 292 · see citing works
Paracrine and Autocrine Functions of Neuronal Vascular Endothelial Growth Factor (VEGF) in the Central Nervous System
Ogunshola, O. O., Antic, A., Donoghue, M. J., Fan, S.-Y., Kim, H., Stewart, W. B., Jr., Madri, J. A., & Ment, L. R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111085200 · Cited by 268 · see citing works
The effects of forced exercise on hippocampal plasticity in the rat: A comparison of LTP, spatial- and non-spatial learning
O'Callaghan, R., OHLE, R., & Kelly, A. M. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.018 · Cited by 268 · see citing works
The neurobiology of memory changes in normal aging
Erickson, C. (2003) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00160-2 · Cited by 267 · see citing works
Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats
Maren, S. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06485.x · Cited by 267 · see citing works
Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington’s disease transgenic mice
Pang, T. Y. C., Stam, N. C., Nithianantharajah, J., Howard, M. L., & Hannan, A. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.013 · Cited by 265 · see citing works
Physical Exercise Protects Against Alzheimer's Disease in 3xTg-AD Mice
García‐Mesa, Y., López, J. C., Giménez‐Llort, L., Revilla, S., Guerra, R., Gruart, A., LaFerla, F. M., Cristòfol, R. M., Delgado-Garcia, J. M., & Sanfeliu, C. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-101635 · Cited by 253 · see citing works
Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus
Redila, V. A., & Christie, B. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.050 · Cited by 235 · see citing works
Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map
Leutgeb, S., & Leutgeb, J. K. (2007) · Learning & Memory · doi:10.1101/lm.703907 · Cited by 234 · see citing works
5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus
Radley, J. J., & Jacobs, B. L. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03477-7 · Cited by 231 · see citing works
Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus
Hattiangady, B., Rao, M. S. R., Shetty, G. A., & Shetty, A. K. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.05.014 · Cited by 230 · see citing works
Exercise improves memory acquisition and retrieval in the Y-maze task: Relationship with hippocampal neurogenesis.
van der Borght, K., Havekes, R., Bos, T., Eggen, B. J. L., & van der Zee, E. A. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.2.324 · Cited by 227 · see citing works
Exercise improves cognition and hippocampal plasticity in APOE ɛ4 mice
Nichol, K., Deeny, S. P., Seif, J., Camaclang, K., & Cotman, C. W. (2009) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2009.02.006 · Cited by 213 · see citing works
Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis
Van der Borght, K., Kóbor‐Nyakas, D. É., Klauke, K., Eggen, B. J. L., Nyakas, C., Van der Zee, E. A., & Meerlo, P. (2009) · Hippocampus · doi:10.1002/hipo.20545 · Cited by 210 · see citing works
Brain-derived neurotrophic factor mechanisms and function in adult synaptic plasticity: new insights and implications for therapy.
Kuipers, S. D., & Bramham, C. R. (2006) · PubMed · Cited by 209 · see citing works
Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons
Tronel, S., Fabre, A., Charrier, V., Oliet, S. H. R., Gage, F. H., & Abrous, D. N. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914613107 · Cited by 207 · see citing works
Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats
Lou, S., Liu, J., Chang, H., & Chen, P. (2008) · Brain Research · doi:10.1016/j.brainres.2008.02.080 · Cited by 206 · see citing works
Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain
Naylor, A. S., Bull, C., Nilsson, M. K. L., Zhu, C., Björk‐Eriksson, T., Eriksson, P. S., Blomgren, K., & Kuhn, H. G. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711128105 · Cited by 205 · see citing works
Exercise enhances the proliferation of neural stem cells and neurite growth and survival of neuronal progenitor cells in dentate gyrus of middle-aged mice
Wu, C.-W. J., Chang, Y.-T., Yu, L., Chen, H., Jen, C. J., Wu, S.-Y., Lo, C., & Kuo, Y. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.90775.2008 · Cited by 204 · see citing works
Exercise induces BDNF and synapsin I to specific hippocampal subfields
Vaynman, S., Ying, Z., & Gómez‐Pinilla, F. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20077 · Cited by 203 · see citing works
The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise
Adlard, P. A., Perreau, V. M., Engesser‐Cesar, C., & Cotman, C. W. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.03.058 · Cited by 202 · see citing works
Disambiguating the similar: The dentate gyrus and pattern separation
Schmidt, B., Marrone, D. F., & Markus, E. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.039 · Cited by 198 · see citing works
The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat
Gold, A., & Kesner, R. P. (2005) · Hippocampus · doi:10.1002/hipo.20103 · Cited by 196 · see citing works
Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments.
Greenough, W. T., Hwang, H.-M., & Gorman, C. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.13.4549 · Cited by 195 · see citing works
Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice
Mustroph, M. L., Chen, S., Desai, S. C., Cay, E. B., DeYoung, E. K., & Rhodes, J. S. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.06.007 · Cited by 190 · see citing works
Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice
Lambert, T. J., Fernandez, S. M., & Frick, K. M. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.12.001 · Cited by 187 · see citing works
Angiogenic and astroglial responses to vascular endothelial growth factor administration in adult rat brain
Krum, J. M., Mani, N., & Rosenstein, J. M. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00615-7 · Cited by 185 · see citing works
Changes in ??-Endorphin Levels in Response to Aerobic and Anaerobic Exercise
Schwarz, L., & Kindermann, W. (1992) · Sports Medicine · doi:10.2165/00007256-199213010-00003 · Cited by 185 · see citing works
Exercise enhances hippocampal‐dependent learning in the rat: Evidence for a BDNF‐related mechanism
Griffin, É. W., Bechara, R. G., Birch, A. M., & Kelly, A. M. (2009) · Hippocampus · doi:10.1002/hipo.20631 · Cited by 168 · see citing works
Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones
Xiao, M., & Hendrickson, A. E. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001002)425:4 · Cited by 165 · see citing works
AMP-activated protein kinase: a key system mediating metabolic responses to exercise
HARDIE, D. G. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000106171.38299.64 · Cited by 165 · see citing works
Three weeks of running wheel exposure improves cognitive performance in the aged Tg2576 mouse
Nichol, K. E., Parachikova, A. I., & Cotman, C. W. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.06.027 · Cited by 160 · see citing works
The influence of exercise on brain aging and dementia
Lautenschlager, N. T., Cox, K. L., & Cyarto, E. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.07.010 · Cited by 157 · see citing works
Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus.
O'Callaghan, R. M., Griffin, É. W., & Kelly, Á. M. (2009) · Hippocampus · doi:10.1002/hipo.20591 · Cited by 146 · see citing works
Enhanced production and dendritic growth of new dentate granule cells in the middle‐aged hippocampus following intracerebroventricular FGF‐2 infusions
Rai, K. S., Hattiangady, B., & Shetty, A. K. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05820.x · Cited by 144 · see citing works
Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning
Fordyce, D. E., & Farrar, R. P. (1991) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80105-6 · Cited by 144 · see citing works
Context, conditioning, and hippocampal rerepresentation in animal learning.
Myers, C. E., & Gluck, M. A. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.5.835 · Cited by 142 · see citing works
Voluntary Running Prevents Progressive Memory Decline and Increases Adult Hippocampal Neurogenesis and Growth Factor Expression after Whole-Brain Irradiation
Wong‐Goodrich, S. J. E., Pfau, M. L., Flores, C., Fraser, J. A., Williams, C. L., & Jones, L. W. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1854 · Cited by 141 · see citing works
Functional analysis of neurovascular adaptations to exercise in the dentate gyrus of young adult mice associated with cognitive gain.
Clark, P. J., Brzezinska, W. J., Puchalski, E. K., Krone, D. A., & Rhodes, J. S. (2009) · Hippocampus · doi:10.1002/hipo.20543 · Cited by 138 · see citing works
Brain-Derived Neurotrophic Factor Signaling Does Not Stimulate Subventricular Zone Neurogenesis in Adult Mice and Rats
Galvão, R. P., García‐Verdugo, J. M., & Álvarez-Buylla, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2918-08.2008 · Cited by 138 · see citing works
Enhancement of neurogenesis by running wheel exercises is suppressed in mice lacking NMDA receptor ε1 subunit
Kitamura, T., Mishina, M., & Sugiyama, H. (2003) · Neuroscience Research · doi:10.1016/s0168-0102(03)00171-8 · Cited by 134 · see citing works
Endogenous cannabinoid signaling is required for voluntary exercise‐induced enhancement of progenitor cell proliferation in the hippocampus
Hill, M. N., Titterness, A. K., Morrish, A. C., Carrier, E. J., Lee, T. T. ‐., Gil‐Mohapel, J., Gorzalka, B. B., Hillard, C. J., & Christie, B. R. (2009) · Hippocampus · doi:10.1002/hipo.20647 · Cited by 129 · see citing works
Short-Term Environmental Enrichment Enhances Adult Neurogenesis, Vascular Network and Dendritic Complexity in the Hippocampus of Type 1 Diabetic Mice
Beauquis, J., Roig, P., Nicola, A. F. D., & Saravia, F. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013993 · Cited by 129 · see citing works
Wheel running from a juvenile age delays onset of specific motor deficits but does not alter protein aggregate density in a mouse model of Huntington's disease
van Dellen, A., Cordery, P., Spires, T., Blakemore, C., & Hannan, A. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-34 · Cited by 123 · see citing works
Different types of exercise induce differential effects on neuronal adaptations and memory performance
Lin, T.-W., Chen, S.-J., Huang, T.-Y., Chang, C.-Y., Chuang, J., Wu, F., Kuo, Y., & Jen, C. J. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.10.006 · Cited by 122 · see citing works
The Recent Understanding of the Neurotrophin’s Role in Skeletal Muscle Adaptation
Sakuma, K., & Yamaguchi, A. (2011) · BioMed Research International · doi:10.1155/2011/201696 · Cited by 120 · see citing works
Endurance factors improve hippocampal neurogenesis and spatial memory in mice
Kobilo, T., Yuan, C., & van Praag, H. (2011) · Learning & Memory · doi:10.1101/lm.2001611 · Cited by 114 · see citing works
Self-citation
Context, conditioning, and hippocampal rerepresentation in animal learning.
Myers, C. E., & Gluck, M. A. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.5.835 · Cited by 113 · see citing works
The Amygdala Modulates Hippocampus-Dependent Context Memory Formation and Stores Cue-Shock Associations.
Huff, N. C., & Rudy, J. W. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.1.53 · Cited by 112 · see citing works
Environmental conditions modulate degeneration and new dendrite growth in cerebellum of senescent rats
Greenough, W. T., McDonald, J. W., Parnisari, R. M., & Camel, J. E. (1986) · Brain Research · doi:10.1016/0006-8993(86)91437-x · Cited by 107 · see citing works
A behavioral analysis of the impact of voluntary physical activity on hippocampus‐dependent contextual conditioning
Greenwood, B. N., Strong, P. V., Foley, T. E., & Fleshner, M. (2008) · Hippocampus · doi:10.1002/hipo.20534 · Cited by 106 · see citing works
Effects of exercise on NMDA receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus
Vasuta, C., Caunt, C., James, R., Samadi, S., Schibuk, E., Kannangara, T., Titterness, A. K., & Christie, B. R. (2007) · Hippocampus · doi:10.1002/hipo.20349 · Cited by 105 · see citing works
Effects of Enriched Environment and Fluid Percussion Injury on Dendritic Arborization within the Cerebral Cortex of the Developing Rat
Ip, E. Y.-Y., Giza, C. C., Griesbach, G. S., & Hovda, D. A. (2002) · Journal of Neurotrauma · doi:10.1089/089771502753754055 · Cited by 105 · see citing works
Upregulation of hippocampal TrkB and synaptotagmin is involved in treadmill exercise-enhanced aversive memory in mice
Liu, Y.-F., Chen, H.-I., Yu, L., Kuo, Y.-M., Wu, F.-S., Chuang, J.-I., Liao, P.-C., & Jen, C. J. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.02.005 · Cited by 98 · see citing works
Forced, moderate-intensity treadmill exercise suppresses apoptosis by increasing the level of NGF and stimulating phosphatidylinositol 3-kinase signaling in the hippocampus of induced aging rats
Chae, C., & Kim, H.-T. (2009) · Neurochemistry International · doi:10.1016/j.neuint.2009.02.024 · Cited by 98 · see citing works
Comparison of neurogenic effects of fluoxetine, duloxetine and running in mice
Marlatt, M. W., Lucassen, P. J., & van Praag, H. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.086 · Cited by 96 · see citing works
Environmental and pharmacological modulations of cellular plasticity: Role in the pathophysiology and treatment of depression
Ota, K. T., & Duman, R. S. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.05.022 · Cited by 94 · see citing works
Myopathy as a first symptom of Huntington's disease in a Marathon runner
Kosinski, C. M., Schlangen, C., Gellerich, F. N., Gizatullina, Z. Z., Deschauer, M., Schiefer, J., Young, A. B., Landwehrmeyer, G. B., Toyka, K. V., Sellhaus, B., et al. (2007) · Movement Disorders · doi:10.1002/mds.21550 · Cited by 89 · see citing works
Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable?
Bekinschtein, P., Oomen, C., Saksida, L., & Bussey, T. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.07.002 · Cited by 86 · see citing works
Measuring cognitive deficits in disabled mice using an automated interactive touchscreen system
Morton, A. J., Skillings, E. A., Bussey, T. J., & Saksida, L. M. (2006) · Nature Methods · doi:10.1038/nmeth1006-767 · Cited by 85 · see citing works
Physical activity fails to rescue hippocampal neurogenesis deficits in the R6/2 mouse model of Huntington's disease
Kohl, Z., Kandasamy, M., Winner, B., Aigner, R., Groß, C., Couillard‐Després, S., Bogdahn, U., Aigner, L., & Winkler, J. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.039 · Cited by 84 · see citing works
Voluntary Running and Environmental Enrichment Restores Impaired Hippocampal Neurogenesis in a Triple Transgenic Mouse Model of Alzheimers Disease
Rodriguez, J. J., Noristani, H. N., Olabarria, M., Fletcher, J. A., Somerville, T. D. D., Yeh, C., & Verkhratsky, A. (2011) · Current Alzheimer Research · doi:10.2174/156720511797633214 · Cited by 83 · see citing works
The role of neurotrophins in muscle under physiological and pathological conditions
Chevrel, G., Hohlfeld, R., & Sendtner, M. (2005) · Muscle & Nerve · doi:10.1002/mus.20444 · Cited by 82 · see citing works
Effects of Exercise on Pavlovian Fear Conditioning.
Baruch, D. E., Swain, R. A., & Helmstetter, F. J. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.5.1123 · Cited by 81 · see citing works
Exercise can rescue recognition memory impairment in a model with reduced adult hippocampal neurogenesis
Lafenêtre, P. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.034.2009 · Cited by 80 · see citing works
Physical exercise can reverse the deficit in fear memory induced by maternal deprivation
Mello, P. B., Benetti, F., Cammarota, M., & Izquierdo, I. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.04.004 · Cited by 71 · see citing works
Exercise is not beneficial and may accelerate symptom onset in a mouse model of Huntington’s disease
Potter, M. C., Yuan, C., Ottenritter, C., Mughal, M. R., & van Praag, H. (2010) · PLoS Currents · doi:10.1371/currents.rrn1201 · Cited by 68 · see citing works
Self-citation
Exercise-induced plasticity of AMPA-type glutamate receptor subunits in the rat brain
Real, C. C., Ferreira, A. F. B., Hernandes, M. S., Britto, L. R. G., & Pires, R. S. (2010) · Brain Research · doi:10.1016/j.brainres.2010.09.060 · Cited by 64 · see citing works
Fibroblast growth factor‐2 deficiency causes defects in adult hippocampal neurogenesis, which are not rescued by exogenous fibroblast growth factor‐2
Werner, S., Unsicker, K., & von Bohlen und Halbach, O. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22680 · Cited by 56 · cited 2× · see citing works
“Neutralization of FGF-2 with an antibody to FGF-2 did not interfere with neurogenesis, suggesting that FGF-2 may operate synergistically in combination with other mechanisms/growth factors to mediate the maturation of new neurons in the adult DG (Werner et al. 2011).”
Background
Voluntary exercise improves both learning and consolidation of cued conditioned fear in C57 mice
Falls, W. A., Fox, J. H., & MacAulay, C. M. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.10.016 · Cited by 52 · see citing works
Voluntary exercise does not enhance long-term potentiation in the adolescent female dentate gyrus
Titterness, A. K., Wiebe, E. C., Kwasnica, A., Keyes, G., & Christie, B. R. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.050 · Cited by 49 · see citing works
In vivo opioid receptor occupation in the rat brain following exercise.
Sforzo, G. A., Seeger, T., Pert, C. B., Pert, A., & Dotson, C. O. (1986) · PubMed · Cited by 48 · see citing works
In vivo opioid receptor occupation in the rat brain following exercise
Sforzo, G. A., SEEGER, T. F., Pert, C. B., Pert, A., & Dotson, C. O. (1986) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198608000-00003 · Cited by 45 · see citing works
Short-term adenosine monophosphate-activated protein kinase activator 5-aminoimidazole-4-carboxamide-1-β-D-ribofuranoside treatment increases the sirtuin 1 protein expression in skeletal muscle.
Suwa, M., Nakano, H., Radák, Z., & Kumagai, S. (2011) · Metabolism: Clinical and Experimental · doi:10.1016/j.metabol.2010.03.003 · Cited by 43 · see citing works
Interpreting the effects of exercise on fear conditioning: The influence of time of day.
Hopkins, M. E., & Bucci, D. J. (2010) · Behavioral Neuroscience · doi:10.1037/a0021200 · Cited by 28 · see citing works
Interferon-α-induced deficits in novel object recognition are rescued by chronic exercise
Fahey, B., Barlow, S. H., Day, J. S., & O’Mara, S. M. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.05.008 · Cited by 24 · see citing works
Gap junctional coupling between progenitor cells of regenerating retina in the adult newt
Chiba, C., & Saito, T. (2000) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(20000205)42:2 · Cited by 19 · see citing works
Strenuous, intensive, long-term exercise does not prevent or delay the onset of Huntington’s disease
Altschuler, E. L. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.04.068 · Cited by 14 · see citing works
Effective connectivity analysis of global and local mental imagery by dynamic causal modeling
Li, J., Sui, D., & Tang, Y. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-s1-p34 · Cited by 14 · see citing works

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Brain-Derived Neurotrophic Factor: A Key Molecule for Memory in the Healthy and the Pathological Brain
Miranda, M., Morici, J. F., Zanoni, M. B., & Bekinschtein, P. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00363 · Cited by 1,416 · see citing works
BDNF: A Key Factor with Multipotent Impact on Brain Signaling and Synaptic Plasticity
Kowiański, P., Lietzau, G., Czuba, E., Waśkow, M., Steliga, A., & Moryś, J. (2018) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-017-0510-4 · Cited by 1,359 · see citing works
Physical activity and depression: towards understanding the antidepressant mechanisms of physical activity
Kandola, A., Ashdown-Franks, G., Hendrikse, J., Sabiston, C. M., & Stubbs, B. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.040 · Cited by 1,309 · see citing works
The effects of acute exercise on mood, cognition, neurophysiology, and neurochemical pathways: a review.
Basso, J. C., & Suzuki, W. A. (2016) · Brain Plasticity · doi:10.3233/bpl-160040 · Cited by 911 · see citing works
Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease
Petzinger, G. M., Fisher, B. E., McEwen, S., Beeler, J. A., Walsh, J. P., & Jakowec, M. W. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70123-6 · Cited by 798 · see citing works
Exercise Attenuates the Major Hallmarks of Aging
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Authors: Vivar, C., Potter, M. C., & van Praag, H.
Affiliations: National Institutes of Health (US)
ORCID: Vivar, Carmen
Potter, Michelle C.
Venue: Current Topics in Behavioral Neurosciences
Publisher: Springer Berlin Heidelberg
Published: 2012
Volume: 15
Pages: 189-210
ISSN: 1866-3370 (ISSN-L)
1866-3389
DOI: 10.1007/7854_2012_220
PMC: PMC4565722
OpenAlex: W2262705777
Semantic Scholar: be1fabad6b4cb0fc07f4ee6b536629bf43d94e04
Cited by: 370
References: 171
Citations by year: 2026: 12 · 2025: 18 · 2024: 19 · 2023: 26 · 2022: 21 · 2021: 33 · 2020: 30 · 2019: 41 · 2018: 28 · 2017: 42 · 2016: 35 · 2015: 30 · 2014: 18 · 2013: 16 · 2012: 1
FWCI: 27.82
Type: book chapter
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Current topics in behavioral neurosciences (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Johns Hopkins University
National Institutes of Health
National Institute on Aging (ZIAAG000328)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: physical activity, adult hippocampal neurogenesis, synaptic plasticity, dentate gyrus, brain-derived neurotrophic factor, growth factors, learning and memory, neurodegenerative diseases, age-related cognitive decline, dendritic spine density, neurotransmission, rodents
MeSH terms: Animals, Cognition, Hippocampus, Synaptic Transmission, Neuronal Plasticity, Running, Neurogenesis

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