Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat.
Abstract
Previous work has shown that voluntary running increases cell proliferation and neurogenesis in the dentate gyrus of the adult hippocampus. Here we report that long-term running for 24 days results in a down-regulation of hippocampal progenitor proliferation to one-half the level of nonrunning controls compared with a fivefold increase in progenitor proliferation seen after 9 days of voluntary running (short-term running). The negative effects seen on proliferation after 24 days of running were prevented by restricting daily running distances (by 30-50%) during 24 days. Long-term running for 24 days increases the response of the hypothalamic-pituitary-adrenal axis, with an increase in adrenal gland weight and increased plasma corticosterone levels, as well as decreased thymus weight, indicating a stress response as a possible mediator of decreased progenitor proliferation. Furthermore, the negative effects seen on the observed stress response after 24 days of running were prevented by restricting daily running distance. Short-term running did not alter these stress parameters compared with nonrunning controls. However, it increased phosphorylated cyclic AMP response element binding protein (pCREB) in the dentate gyrus, an increase that was not seen in nonrunning controls or after 24 days of running. Taken together, these data suggest that voluntary running does not always enhance proliferation and that the decrease in progenitor proliferation seen in long-term running is possibly mediated by mechanisms involving a stress response in the animal. However, a moderate level of long-term running was able to prevent the negative stress-related changes seen in unrestricted long-term running.
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“Using hippocampus dependent paradigms, AE has been reliably demonstrated to improve task performance in animal models (van Praag, 2009; Voss et al., 2013a), although this does also depend on others aspects of AE such as the duration and intensity of AE (Naylor et al., 2005; Ploughman et al., 2007; O’Callaghan et al., 2009).”
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 Naylor et al., 2005
Cites
Neurogenesis in the adult human hippocampus
Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.-M., Nordborg, C., Peterson, D. A., & Gage, F. H. (1998) · Nature Medicine · doi:10.1038/3305 · Cited by 6,369 · see citing works
Self-citationRunning increases cell proliferation and neurogenesis in the adult mouse dentate gyrus
van Praag, H., Kempermann, G., & Gage, F. H. (1999) · Nature Neuroscience · doi:10.1038/6368 · Cited by 3,880 · see citing works
Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats
Altman, J., & Das, G. D. (1965) · Journal of Comparative Neurology · doi:10.1002/cne.901240303 · Cited by 3,592 · see citing works
GUNDERSEN, H. J. G., BENDTSEN, T. F., KORBO, L., MARCUSSEN, N., MØLLER, A., NIELSEN, K., NYENGAARD, J. R., PAKKENBERG, B., SØRENSEN, F. B., VESTERBY, A., et al. (1988) · APMIS · doi:10.1111/j.1699-0463.1988.tb05320.x · Cited by 2,929 · see citing works
Running enhances neurogenesis, learning, and long-term potentiation in mice
van Praag, H., Christie, B. R., Sejnowski, T. J., & Gage, F. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13427 · Cited by 2,904 · see citing works
Learning enhances adult neurogenesis in the hippocampal formation
Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999) · Nature Neuroscience · doi:10.1038/6365 · Cited by 2,157 · see citing works
Hippocampal atrophy in recurrent major depression
Sheline, Y. I., Wang, P. W., Gado, M. H., Csernansky, J. G., & Vannier, M. W. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.9.3908 · Cited by 1,932 · see citing works
The stressed hippocampus, synaptic plasticity and lost memories
Kim, J. J., & Diamond, D. M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn849 · Cited by 1,543 · see citing works
Trejo, J. L., Carro, E., & Torres-Alemán, I. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01628.2001 · Cited by 1,017 · see citing works
Neeper, S. A., Gómez‐Pinilla, F., Choi, J., & Cotman, C. W. (1996) · Brain Research · doi:10.1016/0006-8993(96)00273-9 · Cited by 1,015 · see citing works
Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus
Cameron, H. A., & Gould, E. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90224-0 · Cited by 999 · see citing works
Adult brain neurogenesis and psychiatry: a novel theory of depression
Jacobs, B. L., van Praag, H., & Gage, F. H. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000712 · Cited by 964 · see citing works
VEGF is necessary for exercise‐induced adult hippocampal neurogenesis
Fabel, K., Fabel, K., Tam, B., Kaufer, D., Baiker, A., Simmons, N., Kuo, C. J., & Palmer, T. D. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03041.x · Cited by 861 · see citing works
Peripheral Infusion of IGF-I Selectively Induces Neurogenesis in the Adult Rat Hippocampus
Åberg, M. A. I., Åberg, N. D., Hedbäcker, H., Oscarsson, J., & Eriksson, P. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-08-02896.2000 · Cited by 852 · see citing works
Self-citationFarmer, J., Zhao, X., van Praag, H., Wodtke, K., Gage, F. H., & Christie, B. R. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.09.029 · Cited by 836 · see citing works
Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity
Gómez-Pinilla, F., Ying, Z., Roy, R. R., Molteni, R., & Edgerton, V. R. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00152.2002 · Cited by 724 · see citing works
Adrenal hormones suppress cell division in the adult rat dentate gyrus
Gould, E., Cameron, H. A., Daniels, D., Woolley, C. S., & McEwen, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-09-03642.1992 · Cited by 652 · see citing works
Carro, E., Trejo, J. L., Busiguina, S., & Torres-Aleman, I. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05678.2001 · Cited by 601 · see citing works
Nakagawa, S., Kim, J., Lee, R., Malberg, J. E., Chen, J., Steffen, C., Zhang, Y., Nestler, E. J., & Duman, R. S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03673.2002 · Cited by 486 · see citing works
Regulation of hippocampal neurogenesis in adulthood
Gould, E., Tanapat, P., Rydel, T. A., & Hastings, N. B. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01021-0 · Cited by 400 · see citing works
Jin, C., & Reed, J. C. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm832 · Cited by 340 · see citing works
Hippocampal Remodeling and Damage by Corticosteroids Implications for Mood Disorders
Brown, E. S. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00054-8 · Cited by 335 · see citing works
Moraska, A. F., Terrence Deak, B., Spencer, R. L., Roth, D., & Fleshner, M. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.4.r1321 · Cited by 325 · see citing works
Effects of Exercise on Gene-Expression Profile in the Rat Hippocampus
Tong, L., Shen, H., Perreau, V. M., Balázs, R., & Cotman, C. W. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2001.0427 · Cited by 325 · see citing works
Effects of long-term voluntary exercise on the mouse hypothalamic–pituitary–adrenocortical axis
Droste, S. K., Gesing, A., Ulbricht, S., Müller, M. B., Linthorst, A. C. E., & Reul, J. M. H. M. (2003) · Endocrinology · doi:10.1210/en.2003-0097 · Cited by 324 · see citing works
Rhodes, J. S., van Praag, H., Jeffrey, S., Girard, I., Mitchell, G. S., Garland, T., & Gage, F. H. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.5.1006 · Cited by 269 · see citing works
Gómez-Oliver, F., Lahmame, A., de Kloet, E. R., & Armario, A. (2008) · Neuroendocrinology · doi:10.1159/000126973 · Cited by 264 · see citing works
Nakagawa, S., Kim, J., Lee, R., Chen, J., Fujioka, T., Malberg, J. E., Tsuji, S., & Duman, R. S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09868.2002 · Cited by 263 · see citing works
Adult hippocampal neurogenesis and voluntary running activity: Circadian and dose‐dependent effects
Holmes, M. M., Galea, L. A. M., Mistlberger, R. E., & Kempermann, G. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20039 · Cited by 233 · see citing works
Any way you cut it: A new journal policy for the use of unbiased counting methods
Saper, C. B. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960101)364:1 · Cited by 226 · see citing works
McEwen, B. S., Gould, E., & Sakai, R. R. (1992) · The British Journal of Psychiatry · doi:10.1192/s0007125000296645 · Cited by 206 · see citing works
Corticosterone: narrow range required for normal body and thymus weight and ACTH
Akana, S. F., Cascio, C. S., Shinsako, J., & Dallman, M. F. (1985) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1985.249.5.r527 · Cited by 199 · see citing works
Glucocorticoid-induced apoptosis in the thymus.
Cohen, J. (1992) · PubMed · Cited by 166 · see citing works
Gould, E., & McEwen, B. S. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90138-o · Cited by 164 · see citing works
Plasticity, Hippocampal Place Cells, and Cognitive Maps
Shapiro, M. L. (2001) · Archives of Neurology · doi:10.1001/archneur.58.6.874 · Cited by 131 · see citing works
Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus
Cameron, H. A., Woolley, C. S., & Gould, E. (1993) · Brain Research · doi:10.1016/0006-8993(93)90524-q · Cited by 129 · see citing works
Differential effects of corticosterone and dexamethasone on hippocampal neurogenesis in vitro
Yu, I. T., Lee, S., Lee, Y.-S., & Son, H. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.03.071 · Cited by 105 · see citing works
Physiological programmed cell death in thymocytes is induced by physical stress (exercise)
Concordet, J., & Ferry, A. (1993) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1993.265.3.c626 · Cited by 95 · see citing works
Rodriguez, J. J., Montaron, M., Petry, K. G., Aurousseau, C., Marinelli, M., Premier, S., Rougon, G. N., Moal, M. L., & Abrous, D. N. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00316.x · Cited by 93 · see citing works
Neural stem cells: From fly to vertebrates
Doe, C. Q., Fuerstenberg, S., & Peng, C. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199808)36:2 · Cited by 85 · see citing works
Interactions between body temperature and wheel running over the estrous cycle in rats.
Kent, S., Hurd, M., & Satinoff, E. (1991) · Physiology and Behavior · doi:10.1016/0031-9384(91)90334-k · Cited by 79 · see citing works
Phorbol ester inhibition of Na-H exchange in rabbit proximal colon
Ahn, J. S., Chang, E. B., & Field, M. (1985) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1985.249.5.c527 · Cited by 76 · see citing works
Persson, A. I., Naylor, A. S., Jónsdóttir, I. H., Nyberg, F., Eriksson, P. S., & Thorlin, T. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03268.x · Cited by 63 · see citing works
Self-citationEnhanced Brain Cell Proliferation Following Early Adrenalectomy in Rats
Yehuda, R., Fairman, K. R., & Meyer, J. S. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb07320.x · Cited by 59 · see citing works
Eriksson, P. S., & Wallin, L. (2004) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.2004.00328.x · Cited by 54 · see citing works
Self-citationReul, J. M. H. M., Bilang‐Bleuel, A., Droste, S. K., Linthorst, A. C. E., Holsboer, F., & Gesing, A. (2000) · Zeitschrift für Rheumatologie · doi:10.1007/s003930070013 · Cited by 21 · see citing works
Hori, T., Fukuda, M., Suzuki, H., Yano, S., & Ono, T. (1993) · Clinical Immunology and Immunopathology · doi:10.1006/clin.1993.1125 · Cited by 21 · see citing works
The significance of intensity and duration of exercise on natural immunity in rats
Jónsdóttir, I. H., & Hoffmann, P. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200011000-00014 · Cited by 16 · see citing works
Effect of stress on organ weight in rats.
Sardessai, S. R., Abraham, M. E., & Jf, M. (1993) · PubMed · Cited by 13 · see citing works
Relation between voluntary physical activity and oxidant/antioxidant status in rats
Yamamoto, T., Ohkuwa, T., Itoh, H., Sato, Y., & Naoi, M. (2003) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/s1532-0456(03)00087-5 · Cited by 12 · see citing works
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Mirescu, C., & Gould, E. (2006) · Hippocampus · doi:10.1002/hipo.20155 · Cited by 701 · see citing works
Olson, A. K., Eadie, B. D., Ernst, C., & Christie, B. R. (2006) · Hippocampus · doi:10.1002/hipo.20157 · Cited by 565 · see citing works
Social isolation delays the positive effects of running on adult neurogenesis
Stranahan, A. M., Khalil, D., & Gould, E. (2006) · Nature Neuroscience · doi:10.1038/nn1668 · Cited by 467 · see citing works
Lucassen, P. J., Meerlo, P., Naylor, A. S., van Dam, A. M., Dayer, A. G., Fuchs, E., Oomen, C. A., & Czéh, B. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.08.003 · Cited by 449 · see citing works
Self-citationGarland, T., Schutz, H., Chappell, M. A., Keeney, B. K., Meek, T. H., Copes, L. E., Acosta, W., Drenowatz, C., Maciel, R. C., van Dijk, G., et al. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.048397 · Cited by 444 · see citing works
Fabel, K. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.22.002.2009 · Cited by 429 · see citing works
Biological Mechanisms of Physical Activity in Preventing Cognitive Decline
Lista, I., & Sorrentino, G. (2009) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-009-9488-x · Cited by 367 · see citing works
Forced and voluntary exercise differentially affect brain and behavior
Leasure, J. L., & Jones, M. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.041 · Cited by 335 · see citing works
Jakubs, K., Nanobashvili, A., Bonde, S., Ekdahl, C. T., Kokaia, Z., Kokaia, M., & Lindvall, O. (2006) · Neuron · doi:10.1016/j.neuron.2006.11.004 · Cited by 250 · see citing works
Central Mechanisms of HPA Axis Regulation by Voluntary Exercise
Stranahan, A. M., Lee, K., & Mattson, M. P. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8027-0 · Cited by 235 · 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
Self-citationHenriksson, H. B., Thornemo, M., Karlsson, C., Hägg, O., Junevik, K., Lindahl, A. H., & Brisby, H. (2009) · Spine · doi:10.1097/brs.0b013e3181a95ad2 · Cited by 202 · see citing works
Uda, M., Ishido, M., Kami, K., & Masuhara, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.05.066 · Cited by 193 · see citing works
Running is rewarding and antidepressive
Brené, S., Bjørnebekk, A., Åberg, E., Mathé, A. A., Olson, L., & Werme, M. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.05.015 · Cited by 172 · see citing works
Ploughman, M., Granter-Button, S., Chernenko, G., Attwood, Z., Tucker, B. A., Mearow, K. M., & Corbett, D. (2007) · Brain Research · doi:10.1016/j.brainres.2007.02.065 · Cited by 170 · see citing works
Lucassen, P. J., Oomen, C. A., Naninck, E. F. G., Fitzsimons, C. P., van Dam, A.-M., Czeh, B., & Korosi, A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021303 · Cited by 166 · see citing works
Adult Hippocampal Neurogenesis: Regulation and Possible Functional and Clinical Correlates
Baptista, P., & Andrade, J. P. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00044 · Cited by 162 · see citing works
The effects of running and of inhibiting adult neurogenesis on learning and memory in rats.
Wojtowicz, J. M., Askew, M. L., & Winocur, G. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06128.x · Cited by 158 · see citing works
Kandola, A., Hendrikse, J., Lucassen, P. J., & Yücel, M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00373 · Cited by 155 · see citing works
“Animal models have shown AE to be associated with a region-specific up-regulation of BDNF in the hippocampus (Neeper et al., 1995; Marlatt et al., 2012; Uysal et al., 2015).”
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
Adult hippocampal neurogenesis and aging
Klempin, F., & Kempermann, G. (2007) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-007-0731-5 · Cited by 139 · see citing works
Pietrelli, A., López‐Costa, J. J., Goñi, R., Brusco, A., & Basso, N. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.054 · Cited by 125 · see citing works
Physical Exercise Alleviates ADHD Symptoms: Regional Deficits and Development Trajectory
Archer, T., & Kostrzewa, R. M. (2011) · Neurotoxicity Research · doi:10.1007/s12640-011-9260-0 · Cited by 123 · see citing works
Littlefield, A. M., Setti, S. E., Priester, C., & Kohman, R. A. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0362-0 · Cited by 121 · see citing works
Activity Dependency and Aging in the Regulation of Adult NeurogenesisPreprint
Kempermann, G. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018929 · Cited by 113 · see citing works
Leasure, J. L., & Decker, L. (2009) · Hippocampus · doi:10.1002/hipo.20563 · Cited by 112 · see citing works
Identification of a stem cell niche in the zone of Ranvier within the knee joint
Karlsson, C., Thornemo, M., Henriksson, H. B., & Lindahl, A. H. (2009) · Journal of Anatomy · doi:10.1111/j.1469-7580.2009.01115.x · Cited by 109 · see citing works
Grégoire, C., Bonenfant, D., Nguyen, A. L., Aumont, A., & Fernandes, K. J. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086237 · Cited by 106 · see citing works
Stress as a Modulator of Motor System Function and Pathology
Metz, G. A. S. (2007) · Reviews in the Neurosciences · doi:10.1515/revneuro.2007.18.3-4.209 · Cited by 106 · see citing works
Running reduces stress and enhances cell genesis in aged mice
Kannangara, T. S., Lucero, M. J., Gil-Mohapel, J., Drapala, R. J., Simpson, J. M., Christie, B. R., & van Praag, H. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.12.025 · Cited by 107 · see citing works
Alomari, M. A., Khabour, O. F., Alzoubi, K. H., & Alzubi, M. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.03.007 · Cited by 107 · see citing works
Ryan, S. M., & Kelly, A. M. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.03.007 · Cited by 104 · see citing works
Kleemeyer, M. M., Kühn, S., Prindle, J., Bodammer, N. C., Brechtel, L., Garthe, A., Kempermann, G., Schaefer, S., & Lindenberger, U. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2015.11.026 · Cited by 98 · see citing works
Llorens-Martı́n, M., Torres‐Alemán, I., & Trejo, J. L. (2006) · Hippocampus · doi:10.1002/hipo.20175 · Cited by 98 · see citing works
Adult Hippocampal Neurogenesis in Natural Populations of MammalsPreprint
Amrein, I. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021295 · Cited by 96 · see citing works
Exercise‐induced promotion of hippocampal cell proliferation requires β‐endorphin
Koehl, M., Meerlo, P., Gonzales, D., Rontal, A., Turek, F. W., & Abrous, D. N. (2008) · The FASEB Journal · doi:10.1096/fj.07-099101 · Cited by 95 · see citing works
Social stress-related behavior affects hippocampal cell proliferation in mice
Mitra, R., Sundlass, K., Parker, K. J., Schatzberg, A. F., & Lyons, D. M. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.05.047 · Cited by 95 · see citing works
Exercise Neuroprotection in a Rat Model of Binge Alcohol Consumption
Leasure, J. L., & Nixon, K. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.01105.x · Cited by 83 · see citing works
Ferrer-Uris, B., Ramos, M. A., Busquets, A., & Angulo-Kinzler, R. M. (2022) · AIMS neuroscience · doi:10.3934/neuroscience.2022009 · Cited by 86 · see citing works
Cerebral Vasomotor Reactivity during Hypo- and Hypercapnia in Sedentary Elderly and Masters Athletes
Zhu, Y.-S., Tarumi, T., Tseng, B. Y., Palmer, D., Levine, B. D., & Zhang, R. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.66 · Cited by 81 · see citing works
Epp, J. R., Barker, J. M., & Galea, L. A. M. (2009) · Hippocampus · doi:10.1002/hipo.20546 · Cited by 80 · see citing works
Liang, J., Wang, C., Zhang, H., Huang, J., Xie, J., & Chen, N. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.755665 · Cited by 66 · see citing works
Voluntary Exercise Increases Oligodendrogenesis in Spinal Cord
Krityakiarana, W., Monteros, A. E. D. L., Ghiani, C. A., Zhao, P. M., Topaldjikian, N., Gómez‐Pinilla, F., Yamaguchi, M., Kotchabhakdi, N., & de Vellis, J. (2010) · International Journal of Neuroscience · doi:10.3109/00207450903222741 · Cited by 65 · see citing works
Bjørnebekk, A., Mathé, A. A., & Brené, S. (2010) · Hippocampus · doi:10.1002/hipo.20683 · Cited by 61 · see citing works
Lee, M. C., Inoue, K., Okamoto, M., Liu, Y. F., Matsui, T., Yook, J. S., & Soya, H. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.01.005 · Cited by 57 · see citing works
Offer and demand: proliferation and survival of neurons in the dentate gyrus
Lehmann, K., Butz, M., & Teuchert, G. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04156.x · Cited by 58 · see citing works
Choi, D., Lee, K. H., & Lee, J. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.4891 · Cited by 52 · see citing works
Developmental dysregulation of adult neurogenesis
Kuhn, H. G., & Blomgren, K. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07610.x · Cited by 49 · see citing works
O’Leary, J. D., Hoban, A. E., Murphy, A., O’Leary, O. F., Cryan, J. F., & Nolan, Y. M. (2018) · Hippocampus · doi:10.1002/hipo.23032 · Cited by 50 · see citing works
Merkley, C. M., Jian, C., Mosa, A. J., Tan, Y., & Wojtowicz, J. M. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00174 · Cited by 47 · see citing works
Anatomical perspectives on adult neural stem cells
Watts, C., McConkey, H. Z. R., Anderson, L., & Caldwell, M. A. (2005) · Journal of Anatomy · doi:10.1111/j.1469-7580.2005.00448.x · Cited by 44 · see citing works
Stress, subjective and objective health
Lundberg, U. (2006) · International Journal of Social Welfare · doi:10.1111/j.1468-2397.2006.00443.x · Cited by 44 · see citing works
Yamaguchi, S., Aoyama, T., Ito, A., Nagai, M., Iijima, H., Tajino, J., Zhang, X., Kiyan, W., & Kuroki, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151580 · Cited by 41 · see citing works
Barbarich-Marsteller, N. C., Fornal, C. A., Takase, L. F., Bocarsly, M. E., Arner, C. N., Walsh, B. T., Hoebel, B. G., & Jacobs, B. L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.047 · Cited by 40 · see citing works
Klaus, F., & Amrein, I. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.027 · Cited by 40 · see citing works
Hippocampal functional hyperemia mediated by NMDA receptor/NO signaling in rats during mild exercise
Nishijima, T., Okamoto, M., Matsui, T., Kita, I., & Soya, H. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00763.2011 · Cited by 38 · see citing works
Kronenberg, G., Lippoldt, A., & Kempermann, G. (2006) · Developmental Neuroscience · doi:10.1159/000096217 · Cited by 37 · see citing works
Robinson, A. M., Hopkins, M. E., & Bucci, D. J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20530 · Cited by 34 · see citing works
Activation of neural precursors in the adult neurogenic niches
Vukovic, J., Blackmore, D. G., Jhaveri, D. J., & Bartlett, P. F. (2011) · Neurochemistry International · doi:10.1016/j.neuint.2011.04.003 · Cited by 35 · see citing works
Ma, X., Hamadeh, M. J., Christie, B. R., Foster, J. A., & Tarnopolsky, M. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036048 · Cited by 34 · see citing works
Larger hippocampus size in women with anorexia nervosa who exercise excessively than healthy women.
Beadle, J. N., Paradiso, S., Brumm, M., Voss, M., Halmi, K., & McCormick, L. M. (2015) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2014.10.013 · Cited by 33 · see citing works
Zhu, C., Huang, Z., Gao, J., Zhang, Y., Wang, X., Karlsson, N., Li, Q., Lannering, B., Björk‐Eriksson, T., Kuhn, H. G., et al. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06413.x · Cited by 33 · see citing works
Physical Exercise Affects Cell Proliferation in Lumbar Intervertebral Disc Regions in Rats
Sasaki, N., Henriksson, H. B., Runesson, E., Larsson, K., Sekiguchi, M., Kikuchi, S., Konno, S., Rydevik, B. L., & Brisby, H. (2012) · Spine · doi:10.1097/brs.0b013e31824ff87d · Cited by 30 · see citing works
Robinson, A. M., Eggleston, R. L., & Bucci, D. J. (2012) · Behavioral Neuroscience · doi:10.1037/a0030488 · Cited by 29 · see citing works
Exercise Duration Differentially Effects Age-related Neuroinflammation and Hippocampal Neurogenesis
Connolly, M. G., Bruce, S. R., & Kohman, R. A. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.03.022 · Cited by 30 · see citing works
Early‐life stress diminishes the increase in neurogenesis after exercise in adult female mice
Abbink, M. R., Naninck, E. F. G., Lucassen, P. J., & Kőrösi, A. (2017) · Hippocampus · doi:10.1002/hipo.22745 · Cited by 29 · see citing works
Li, A., Yau, S.-Y., Machado, S., Wang, P., Yuan, T.-F., & So, K.-F. (2019) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527318666190308102804 · Cited by 27 · see citing works
Seetharaman, S., Fleshner, M., Park, C. R., & Diamond, D. M. (2016) · Brain and Behavior · doi:10.1002/brb3.458 · Cited by 26 · see citing works
An exercise “sweet spot” reverses cognitive deficits of aging by growth-hormone-induced neurogenesis
Blackmore, D. G., Steyn, F. J., Carlisle, A., O’Keeffe, I., Vien, K.-Y., Zhou, X. A., Leiter, O., Jhaveri, D. J., Vukovic, J., Waters, M. J., et al. (2021) · iScience · doi:10.1016/j.isci.2021.103275 · Cited by 24 · see citing works
Ávila‐Gámiz, F., Pérez-Cano, A. M., Pérez-Berlanga, J. M., Mullor-Vigo, R. M., Zambrana-Infantes, E. N., Santín, L. J., & de Guevara‐Miranda, D. L. (2023) · Physiology & Behavior · doi:10.1016/j.physbeh.2023.114184 · Cited by 25 · see citing works
Allen, A. R., Eilertson, K. E., Chakraborti, A., Sharma, S., Baure, J., Habdank-Kolaczkowski, J., Allen, B. D., Rosi, S., Raber, J., & Fike, J. R. (2013) · International Journal of Radiation Biology · doi:10.3109/09553002.2014.859761 · Cited by 25 · see citing works
Åberg, E., Perlmann, T., Olson, L., & Brené, S. (2008) · Hippocampus · doi:10.1002/hipo.20438 · Cited by 25 · see citing works
Postischemic exercise decreases neurogenesis in the adult rat dentate gyrus
Yagita, Y., Kitagawa, K., Sasaki, T., Terasaki, Y., Todo, K., Omura‐Matsuoka, E., Matsumoto, M., & Hori, M. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.09.040 · Cited by 24 · see citing works
The Effects of Exercise Intensity on p-NR2B Expression in Cerebral Ischemic Rats
Zhang, A., Bai, Y., Hu, Y., Zhang, F., Wu, Y., Wang, Y., Zheng, P., & He, Q. (2012) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100015341 · Cited by 23 · see citing works
Spanswick, S. C., Epp, J. R., & Sutherland, R. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.023 · Cited by 22 · see citing works
Grégoire, C., Tobin, S. W., Goldenstein, B., Samarut, É., Leclerc, A., Aumont, A., Drapeau, P., Fulton, S. E., & Fernandes, K. J. L. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00126 · Cited by 22 · see citing works
Cahill, S. P., Cole, J. D., Yu, R. Q., Clemans-Gibbon, J., & Snyder, J. S. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.08.028 · Cited by 22 · see citing works
Nguemeni, C., McDonald, M. W., Jeffers, M. S., Livingston‐Thomas, J. M., Lagace, D. C., & Corbett, D. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.11.026 · Cited by 20 · see citing works
Fan, R., Gong, H., Qiu, S., Zhang, X., Fang, J., & Zhu, D. (2015) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-015-0686-z · Cited by 19 · see citing works
An angiotensin II receptor antagonist suppresses running-enhanced hippocampal neurogenesis in rat
Mukuda, T., & Sugiyama, H. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.02.005 · Cited by 19 · see citing works
Hosseinzadeh, S., Roshan, V. D., & Pourasghar, M. (2013) · Europe PMC (PubMed Central) · Cited by 19 · see citing works
Tauber, S. C., Bunkowski, S., Schlumbohm, C., Rühlmann, M., Fuchs, E., Nau, R., & Gerber, J. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2008.00149.x · Cited by 18 · see citing works
Lee, S., Kim, Y. S., Jun, T.-W., Seo, J.-H., Kim, K.-J., Shin, M., & Kim, C. (2013) · Journal of Exercise Rehabilitation · doi:10.12965/jer.130069 · Cited by 17 · see citing works
Castilla‐Ortega, E., Rosell‐Valle, C., Blanco, E., Pedraza, C., Chun, J. J. M., de Fonseca, F. R., Estivill‐Torrús, G., & Santín, L. J. (2013) · Neuroscience Research · doi:10.1016/j.neures.2013.09.004 · Cited by 17 · see citing works
Robinson, A. M., & Bucci, D. J. (2014) · Behavioral Neuroscience · doi:10.1037/bne0000015 · Cited by 16 · see citing works
Kaiser, A., Reneman, L., Solleveld, M. M., Coolen, B. F., Scherder, E., Knutsson, L., Bjørnerud, A., van Osch, M. J. P., Wijnen, J. P., Lucassen, P. J., et al. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.780095 · Cited by 15 · see citing works
Adult Neurogenesis, Chronic Stress and Depression
Lucassen, P. J., Oomen, C. A., Schouten, M., Encinas, J. M., & Fitzsimons, C. P. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801977-1.00008-8 · Cited by 15 · see citing works
Impact of enriched environment on motor performance and learning in mice
Dijkhuizen, S., Ginneken, L. M. C. V., Ijpelaar, A. C. H. G., Koekkoek, S. K. E., Zeeuw, C. I. D., & Boele, H. (2024) · Scientific Reports · doi:10.1038/s41598-024-56568-3 · Cited by 14 · see citing works
The effects of two forms of physical activity on eyeblink classical conditioning
Green, J. T., Chess, A. C., Burns, M., Schachinger, K. M., & Thanellou, A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.01.016 · Cited by 12 · see citing works
Alkelai, A., Baum, A. E., Carless, M. A., Crowley, J. J., DasBanerjee, T., Dempster, E. L., Docherty, S. J., Hare, E., Galsworthy, M. J., Grover, D., et al. (2008) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30711 · Cited by 12 · see citing works
Larivee, R., Johnson, N., Freedgood, N. R., Cameron, H. A., & Schoenfeld, T. J. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.940125 · Cited by 12 · see citing works
Tamakoshi, K., Ishida, K., Hayao, K., Takahashi, H. E., & Tamaki, H. (2018) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2018.08.038 · Cited by 11 · see citing works
Intermittent individual housing increases survival of newly proliferated cells
Åberg, E., Pham, T. M., Zwart, M., Baumans, V., & Brené, S. (2005) · Neuroreport · doi:10.1097/01.wnr.0000177013.29355.e0 · Cited by 11 · see citing works
Spanswick, S. C., Lehmann, H., & Sutherland, R. J. (2011) · BioMed Research International · doi:10.1155/2011/527201 · Cited by 10 · see citing works
Exploring the neuroprotective role of physical activity in cerebral small vessel disease
Anderson, M. E., Wind, E. J., & Robison, L. S. (2024) · Brain Research · doi:10.1016/j.brainres.2024.148884 · Cited by 8 · see citing works
Bull, C., Cooper, C., Lindahl, V., Fitting, S., Persson, A. I., Grandér, R., Alborn, A., Björk‐Eriksson, T., Kuhn, H. G., & Blomgren, K. (2017) · Radiation Research · doi:10.1667/rr14737.1 · Cited by 7 · see citing works
Self-citationCampos, D. V., Lopim, G. M., de Almeida, V. S., Amado, D., & Arida, R. M. (2016) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2016.08.011 · Cited by 7 · see citing works
Bengoetxea, H., Ortuzar, N., Rico‐Barrio, I., Lafuente, J. V., & Argandoña, E. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00170 · Cited by 7 · see citing works
Mottolese, N., Uguagliati, B., Tassinari, M., Cerchier, C. B., Loi, M., Candini, G., Rimondini, R., Medici, G., Trazzi, S., & Ciani, E. (2023) · Biomolecules · doi:10.3390/biom13091396 · Cited by 6 · see citing works
Brisby, H., Papadimitriou, N., Runesson, E., Sasaki, N., Lindahl, A. H., & Henriksson, H. B. (2013) · Cells Tissues Organs · doi:10.1159/000355919 · Cited by 6 · see citing works
- Authors
- Naylor, A. S., Persson, A. I., Eriksson, P. S., Jonsdottir, I. H., & Thorlin, T.
- Affiliations
- University of Gothenburg (SE)
- ORCID
- Persson, Anders I.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2005-05
- Volume
- 93
- Issue
- 5
- Pages
- 2406-2414
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2054113947
- Cited by
- 127
- References
- 50
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 3 · 2019: 1 · 2018: 5 · 2017: 6 · 2016: 8 · 2015: 7 · 2014: 4 · 2013: 12 · 2012: 6
- FWCI
- 1.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- voluntary running, adult neurogenesis, dentate gyrus, spontaneously hypertensive rats, hypothalamic-pituitary-adrenal axis, corticosterone, stress response, thymus, CREB phosphorylation, exercise duration
- MeSH terms
- Adrenal Glands, Analysis of Variance, Animals, Animals, Newborn, Behavior, Animal, Bromodeoxyuridine, Cell Count, Corticosterone, Female, Hippocampus, Immunohistochemistry, Inhibition, Psychological, Phosphorylation, Physical Conditioning, Animal, Random Allocation, Rats, Inbred SHR, Running, Stem Cells, Thymus Gland, Time Factors, Cyclic AMP Response Element-Binding Protein, Cell Proliferation, Rats
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