Voluntary exercise induces anxiety‐like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis
Abstract
Several studies investigated the effect of physical exercise on emotional behaviors in rodents; resulting findings however remain controversial. Despite the accepted notion that voluntary exercise alters behavior in the same manners as antidepressant drugs, several studies reported opposite or no effects at all. In an attempt to evaluate the effect of physical exercise on emotional behaviors and brain plasticity, we individually housed C57BL/6J male mice in cages equipped with a running wheel. Three weeks after continuous voluntary running we assessed their anxiety‐ and depression‐like behaviors. Tests included openfield, dark‐light‐box, elevated O‐maze, learned helplessness, and forced swim test. We measured corticosterone metabolite levels in feces collected over a 24‐h period and brain‐derived neurotrophic factor (BDNF) in several brain regions. Furthermore, cell proliferation and adult hippocampal neurogenesis were assessed using Ki67 and Doublecortin. Voluntary wheel running induced increased anxiety in the openfield, elevated O‐maze, and dark‐light‐box and higher levels of excreted corticosterone metabolites. We did not observe any antidepressant effect of running despite a significant increase of hippocampal neurogenesis and BDNF. These data are thus far the first to indicate that the effect of physical exercise in mice may be ambiguous. On one hand, the running‐induced increase of neurogenesis and BDNF seems to be irrelevant in tests for depression‐like behavior, at least in the present model where running activity exceeded previous reports. On the other hand, exercising mice display a more anxious phenotype and are exposed to higher levels of stress hormones such as corticosterone. Intriguingly, numbers of differentiating neurons correlate significantly with anxiety parameters in the openfield and dark‐light‐box. We therefore conclude that adult hippocampal neurogenesis is a crucial player in the genesis of anxiety. © 2009 Wiley‐Liss, Inc.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Previous studies have shown an increased anxiety-like phenotype in consequence of increased neurogenesis induced by voluntary wheel running.
“Moreover, previous studies have shown an increased anxiety-like phenotype in consequence of increased neurogenesis induced by voluntary wheel running.37, 38, 39”
From Adult hippocampal neuroplasticity triggers susceptibility to recurrent depression (2017) · cites this paper as [37]
Cites
Gray, J. A. (1982) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00013066 · Cited by 4,477 · see citing works
Running 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
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · 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
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
Hippocampal volume and depression: a meta-analysis of MRI studies
Videbech, P., & Ravnkilde, B. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.11.1957 · Cited by 1,590 · see citing works
Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior
Chen, Z.-Y., Jing, D., Bath, K. G., Ieraci, A., Khan, T., Siao, C.-J., Herrera, D. G., Toth, M., Yang, C., McEwen, B. S., et al. (2006) · Science · doi:10.1126/science.1129663 · Cited by 1,340 · see citing works
A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance
McNaughton, N., & Corr, P. J. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.03.005 · Cited by 1,308 · see citing works
Adult hippocampal neurogenesis in depression
Sahay, A., & Hen, R. (2007) · Nature Neuroscience · doi:10.1038/nn1969 · Cited by 1,206 · see citing works
Exercise and brain neurotrophins
Neeper, S. A., Góauctemez-Pinilla, F., Choi, J., & Cotman, C. (1995) · Nature · doi:10.1038/373109a0 · Cited by 1,066 · see citing works
Aerobic fitness is associated with hippocampal volume in elderly humans
Erickson, K. I., Prakash, R. S., Voss, M. W., Chaddock, L., Hu, L., Morris, K. S., White, S. M., Wójcicki, T. R., McAuley, E., & Kramer, A. F. (2009) · Hippocampus · doi:10.1002/hipo.20547 · Cited by 1,007 · see citing works
Lee, J., Duan, W., & Mattson, M. P. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01085.x · Cited by 975 · see citing works
Doublecortin expression levels in adult brain reflect neurogenesis
Couillard‐Després, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., Bogdahn, U., Winkler, J., Kuhn, H. G., & Aigner, L. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03813.x · Cited by 967 · see citing works
Farmer, 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
The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis
Kee, N., Sivalingam, S., Boonstra, R., & Wojtowicz, J. M. (2002) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(02)00007-9 · Cited by 775 · see citing works
Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C., & Croll, S. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2004.11.016 · Cited by 719 · see citing works
Essential role of brain-derived neurotrophic factor in adult hippocampal function
Monteggia, L. M., Barrot, M., Powell, C. M., Berton, O., Galanis, V., Gemelli, T., Meuth, S., Nagy, A., Greene, R. W., & Nestler, E. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402141101 · Cited by 685 · see citing works
Neural stem cell proliferation is decreased in schizophrenia, but not in depression
Reif, A., Fritzen, S., Finger, M., Strobel, A., Lauer, M., Schmitt, A., & Lesch, K.-P. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001791 · Cited by 630 · see citing works
Touma, C., Sachser, N., Möstl, E., & Palme, R. (2003) · General and Comparative Endocrinology · doi:10.1016/s0016-6480(02)00620-2 · Cited by 581 · see citing works
Self-citationMonteggia, L. M., Luikart, B., Barrot, M., Theobold, D., Malkovska, I., Nef, S., Parada, L. F., & Nestler, E. J. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.021 · Cited by 502 · see citing works
Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice
Duman, C. H., Schlesinger, L., Russell, D. S., & Duman, R. S. (2008) · Brain Research · doi:10.1016/j.brainres.2007.12.047 · Cited by 465 · see citing works
Touma, C., Palme, R., & Sachser, N. (2003) · Hormones and Behavior · doi:10.1016/j.yhbeh.2003.07.002 · Cited by 370 · see citing works
Self-citationGreenwood, B. N., Foley, T. E., Day, H. E. W., Campisi, J., Hammack, S. E., Campeau, S., Maier, S. F., & Fleshner, M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02889.2003 · 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
Govindarajan, A., Rao, B. S. S., Nair, D., Trinh, M. A., Mawjee, N., Tonegawa, S., & Chattarji, S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605180103 · Cited by 332 · 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
Müller, U. (1994) · Cell · doi:10.1016/0092-8674(94)90066-3 · Cited by 308 · see citing works
Leuner, B., Mendolia‐Loffredo, S., Kozorovitskiy, Y., Samburg, D., Gould, E., & Shors, T. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0204-04.2004 · Cited by 289 · 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
Corticosterone response to the plus-mazeHigh correlation with risk assessment in rats and mice
Rodgers, R. J., Haller, J., Holmes, A., Halász, J., WALTON, T., & Brain, P. F. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00140-7 · Cited by 261 · see citing works
Genetic influence on daily wheel running activity level.
Lightfoot, J., Turner, M. J., Daves, M., Vordermark, A., & Kleeberger, S. (2004) · Physiological Genomics · doi:10.1152/physiolgenomics.00125.2004 · Cited by 259 · see citing works
Restoring theta‐like rhythmicity in rats restores initial learning in the Morris water maze
McNaughton, N., Ruan, M., & Woodnorth, M. (2006) · Hippocampus · doi:10.1002/hipo.20235 · Cited by 255 · see citing works
Adult Neurogenesis, Mental Health, and Mental Illness: Hope or Hype?: Figure 1.
Eisch, A. J., Cameron, H. A., Encinas, J. M., Meltzer, L. A., Ming, G., & Overstreet‐Wadiche, L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3798-08.2008 · Cited by 247 · see citing works
Clark, P., Brzezinska, W. J., Thomas, M. W., Ryzhenko, N. A., Toshkov, S. A., & Rhodes, J. S. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.051 · Cited by 236 · see citing works
Exercise Training in Coronary Artery Disease and Coronary Vasomotion
Gielen, S., Schuler, G. C., & Hambrecht, R. (2001) · Circulation · doi:10.1161/01.cir.103.1.e1 · Cited by 231 · see citing works
Learned helplessness: Validity and reliability of depressive-like states in mice
Chourbaji, S., Zacher, C., Sanchis-Segura, C., Dormann, C., Vollmayr, B., & Gass, P. (2005) · Brain Research Protocols · doi:10.1016/j.brainresprot.2005.09.002 · Cited by 216 · see citing works
Self-citationSelective Serotonin-Reuptake Inhibitors: An Update
Masand, P. S., & Gupta, S. (1999) · Harvard Review of Psychiatry · doi:10.3109/hrp.7.2.69 · Cited by 211 · see citing works
The effects of chronic treadmill and wheel running on behavior in rats
Burghardt, P. R., Fulk, L. J., Hand, G. A., & Wilson, M. A. (2004) · Brain Research · doi:10.1016/j.brainres.2004.05.086 · Cited by 204 · see citing works
Balu, D. T., Hoshaw, B. A., Malberg, J. E., Rosenzweig-Lipson, S., Schechter, L. E., & Lucki, I. (2008) · Brain Research · doi:10.1016/j.brainres.2008.03.023 · Cited by 194 · see citing works
Environmental novelty is signaled by reduction of the hippocampal theta frequency
Jeewajee, A., Lever, C., Burton, S., O'Keefe, J. M., & Burgess, N. (2007) · Hippocampus · doi:10.1002/hipo.20394 · Cited by 189 · see citing works
Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice
Binder, E., Droste, S. K., Ohl, F., & Reul, J. M. H. M. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.04.017 · Cited by 188 · see citing works
Cognitive Dysfunction Resulting from Hippocampal Hyperactivity—A Possible Cause of Anxiety Disorder?
McNaughton, N. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00419-4 · Cited by 187 · see citing works
Plasma corticosterone response to acute and chronic voluntary exercise in female house mice
Girard, I., & Garland, T. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00465.2001 · Cited by 176 · 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
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
Deltheil, T., Guiard, B. P., Cerdan, J., David, D. J., Tanaka, K. F., Repérant, C., Guilloux, J.-P., Coudoré, F., Hen, R., & Gardier, A. M. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.08.001 · Cited by 153 · see citing works
Barrós‐Loscertales, A., Meseguer, V., Sanjuán, A., Belloch, V., Parcet, M. A., Torrúbia, R., & Ávila, C. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.07.025 · Cited by 151 · see citing works
Hippocampal morphometry in depressed patients and control subjects: relations to anxiety symptoms
Rusch, B. D., Abercrombie, H. C., Oakes, T. R., Schaefer, S. M., & Davidson, R. J. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01248-3 · Cited by 139 · see citing works
Voluntary exercise in C57 mice is anxiolytic across several measures of anxiety
Salam, J., FOX, J., DETROY, E., GUIGNON, M., Wohl, D. A., & Falls, W. A. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.07.036 · Cited by 139 · see citing works
Malisch, J. L., Breuner, C. W., Gomes, F. R., Chappell, M. A., & Garland, T. (2008) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2008.01.020 · Cited by 130 · see citing works
The role of voluntary exercise in enriched rearing: A behavioral analysis.
Pietropaolo, S., Feldon, J., Alleva, E., Cirulli, F., & Yee, B. K. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.4.787 · Cited by 112 · see citing works
Greenwood, B. N., Strong, P. V., Foley, T. E., & Fleshner, M. (2008) · Hippocampus · doi:10.1002/hipo.20534 · Cited by 106 · see citing works
Chourbaji, S., Zacher, C., Sanchis‐Segura, C., Spanagel, R., & Gass, P. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.003 · Cited by 106 · see citing works
Self-citationHoomissen, J. D. V., Holmes, P. V., Zellner, A. S., Poudevigne, A., & Dishman, R. K. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.6.1378 · Cited by 105 · see citing works
van der Borght, K., Ferrari, F., Klauke, K., Román, V., Havekes, R., Sgoifo, A., van der Zee, E. A., & Meerlo, P. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.08.012 · Cited by 101 · see citing works
Exercising our brains: how physical activity impacts synaptic plasticity in the dentate gyrus.
Christie, B. R., Eadie, B. D., Kannangara, T. S., Robillard, J. M., Shin, J., & Titterness, A. K. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8033-2 · Cited by 99 · see citing works
Cognitive Role of Neurogenesis in Depression and Antidepressant Treatment
Perera, T. D., Park, S., & Nemirovskaya, Y. (2008) · The Neuroscientist · doi:10.1177/1073858408317242 · Cited by 99 · see citing works
Anxiety and Hippocampus Volume in the Rat
Kalisch, R., Schubert, M., Jacob, W., Keßler, M. S., Hemauer, R., Wigger, A., Landgraf, R., & Auer, D. P. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300910 · 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
Endl, E., & Gerdes, J. (2000) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(200003)182:3 · Cited by 89 · see citing works
Neuroprotection and neuronal dysfunction upon repetitive inhibition of oxidative phosphorylation
Hellweg, R., Arnim, C. A. F. V., Büchner, M., Huber, R., & Riepe, M. W. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00127-4 · Cited by 86 · see citing works
Self-citationCherbuin, N., Windsor, T. D., Anstey, K. J., Maller, J. J., Meslin, C., & Sachdev, P. S. (2008) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsn018 · Cited by 82 · see citing works
Effect of access to a running wheel on behavior of C57BL/6J mice.
Harri, M. N. E., Lindblom, J., Malinen, H., Hyttinen, M., Lapveteläinen, T., Eskola, S., & Helminen, H. J. (1999) · PubMed · Cited by 74 · see citing works
Yee, B. K., Zhu, S., Mohammed, A. H., & Feldon, J. (2006) · Journal of Neural Transmission · doi:10.1007/s00702-006-0548-9 · Cited by 73 · see citing works
Pinnock, S. B., & Herbert, J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06250.x · Cited by 62 · see citing works
Abdallah, N. M. ‐. B., Slomianka, L., & Lipp, H. (2007) · Hippocampus · doi:10.1002/hipo.20358 · Cited by 57 · see citing works
Effect of the exercise-induced increase in glucocorticoids on endurance in the rat
Sellers, T. L., Jaussi, A. W., Yang, H., Heninger, R. W., & Winder, W. W. (1988) · Journal of Applied Physiology · doi:10.1152/jappl.1988.65.1.173 · Cited by 56 · see citing works
Kannangara, T. S., Webber, A. J., Gil‐Mohapel, J., & Christie, B. R. (2008) · Hippocampus · doi:10.1002/hipo.20514 · Cited by 46 · see citing works
Bronikowski, A. M., Morgan, T. J., Garland, T., & Carter, P. A. (2006) · Evolution · doi:10.1554/05-590.1 · Cited by 41 · see citing works
Adult Hippocampal Neurogenesis
Kempermann, G. (2010) · Oxford University Press eBooks · doi:10.1093/med/9780199729692.003.0006 · Cited by 27 · see citing works
Non‐spatial expertise and hippocampal gray matter volume in humans
Woollett, K., Glensman, J., & Maguire, E. A. (2008) · Hippocampus · doi:10.1002/hipo.20465 · Cited by 26 · see citing works
Chourbaji, S., Chourbaji, S., Brandwein, C., et al. (2008) · Stress · doi:10.1080/10253890701560119 · Cited by 22 · see citing works
Neurogenesis of the cholinergic medial septum in female and male C57BL/6J mice
Schaevitz, L. R., & Berger-Sweeney, J. E. (2005) · Journal of Neurobiology · doi:10.1002/neu.20188 · Cited by 10 · see citing works
Fritzen, S., Strobel, A., Schmitt, A., Lesch, K., & Reif, A. (2006) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(06)80019-2 · Cited by 10 · see citing works
Imaging new neurons in vivo: a pioneering tool to study the cellular biology of depression?
Römer, B., Sartorius, A., Inta, D., Vollmayr, B., & Gass, P. (2008) · BioEssays · doi:10.1002/bies.20800 · Cited by 5 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Potential therapeutic uses of BDNF in neurological and psychiatric disorders
Nagahara, A. H., & Tuszynski, M. H. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3366 · Cited by 867 · see citing works
Yau, S. Y., Li, A., Hoo, R. L. C., Ching, Y. P., Christie, B. R., Lee, T. M. C., Xu, A., & So, K.-F. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415219111 · Cited by 326 · see citing works
Petrik, D., Lagace, D. C., & Eisch, A. J. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.09.003 · Cited by 241 · see citing works
A runner's high depends on cannabinoid receptors in mice
Fuss, J., Steinle, J., Bindila, L., Auer, M. K., Kirchherr, H., Lutz, B., & Gass, P. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514996112 · Cited by 229 · see citing works
Self-citationAshcraft, K. A., Peace, R. M., Betof, A. S., Dewhirst, M. W., & Jones, L. W. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-0887 · Cited by 217 · see citing works
Brocardo, P. S., Boehme, F., Patten, A., Cox, A., Gil-Mohapel, J., & Christie, B. R. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.10.006 · Cited by 186 · see citing works
Short, A. K., Yeshurun, S., Powell, R., Perreau, V. M., Fox, A., Kim, J. H., Pang, T. Y., & Hannan, A. J. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.82 · Cited by 166 · see citing works
Moylan, S., Eyre, H. A., Maes, M., Baune, B. T., Jacka, F. N., & Berk, M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.003 · Cited by 155 · see citing works
Uysal, N., Kiray, M., Sisman, A., Camsari, U., Gencoglu, C., Baykara, B., Cetinkaya, C., & Aksu, I. (2015) · Biotechnic & Histochemistry · doi:10.3109/10520295.2014.946968 · Cited by 154 · see citing works
Schoenfeld, T. J., Rada, P., Pieruzzini, P. R., Hsueh, B., & Gould, E. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5352-12.2013 · Cited by 138 · see citing works
Early prenatal exposure to LPS results in anxiety- and depression-related behaviors in adulthood
Depino, A. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.065 · Cited by 132 · see citing works
Groves, J. O., Leslie, I., Huang, G.-J., McHugh, S. B., Taylor, A., Mott, R., Munafò, M., Bannerman, D. M., & Flint, J. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003718 · Cited by 121 · see citing works
Kiuchi, T., Lee, H., & Mikami, T. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.01.023 · Cited by 116 · see citing works
The effects of physical exercise in schizophrenia and affective disorders.
Malchow, B., Reich-Erkelenz, D., Oertel-Knöchel, V., Keller, K., Hasan, A., Schmitt, A., Scheewe, T. W., Cahn, W., Kahn, R. S., & Falkai, P. (2013) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-013-0423-2 · Cited by 111 · see citing works
Fuss, J., Ben Abdallah, N. M. B., Hensley, F. W., Weber, K.-J., Hellweg, R., & Gass, P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012769 · Cited by 110 · see citing works
“, recent evidence also indicates that the genesis of new cells in the subgranular zone of the dentate gyrus is part of the biological underpinnings mediating anxiety. Indeed, several gain and loss-of-function studies in adult rodents reported an effect of hippocampal neurogenesis on anxiety behavior”
BackgroundSelf-citationAdult hippocampal neuroplasticity triggers susceptibility to recurrent depression
Alves, N. D., Correia, J. S., Patrício, P., Mateus-Pinheiro, A., Machado-Santos, A. R., Loureiro-Campos, E., Morais, M., Bessa, J. M., Sousa, N., & Pinto, L. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.29 · Cited by 79 · see citing works
Li, H., Liang, A., Guan, F., Fan, R., Chi, L., & Yang, B. (2013) · Brain Research · doi:10.1016/j.brainres.2013.07.041 · Cited by 67 · see citing works
Huang, P., Dong, Z., Huang, W., Zhou, C., Zhong, W., Hu, P., Wen, G., Sun, X., Hua, H., Cao, H., et al. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.05.032 · Cited by 54 · see citing works
Castilla-Ortega, E., Rosell-Valle, C., Pedraza, C., Rodríguez de Fonseca, F., Estivill-Torrús, G., & Santín, L. J. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.001 · Cited by 41 · see citing works
Zhang, Y., Li, G., Liu, C., Guan, J., Zhang, Y., & Shi, Z. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1199510 · Cited by 38 · see citing works
Fuss, J., Biedermann, S. V., Falfán-Melgoza, C., Auer, M. K., Zheng, L., Steinle, J., Hörner, F., Sartorius, A., Ende, G., Weber-Fahr, W., et al. (2014) · Hippocampus · doi:10.1002/hipo.22227 · Cited by 32 · see citing works
Self-citationRunning‐induced anxiety is dependent on increases in hippocampal neurogenesis
Onksen, J. L., Briand, L. A., Galante, R. J., Pack, A. I., & Blendy, J. A. (2012) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2012.00788.x · Cited by 29 · see citing works
Barr, A. M., Wu, C. H., Wong, C., Hercher, C., Töpfer, E., Boyda, H. N., Procyshyn, R. M., Honer, W. G., & Beasley, C. L. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.10.010 · Cited by 26 · see citing works
Greenwood, B. N., Strong, P. V., & Fleshner, M. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.012 · Cited by 24 · see citing works
- Authors
- Fuss, J., Ben Abdallah, N. M. ‐., Vogt, M. A., Touma, C., Pacifici, P. G., Palme, R., Witzemann, V., Hellweg, R., & Gass, P.
- Affiliations
- Central Institute of Mental Health (DE)
- Max Planck Institute of Psychiatry (DE)
- Max Planck Institute for Medical Research (DE)
- University of Veterinary Medicine Vienna (AT)
- Stiftung Charité (DE)
- Corresponding author
- Gass, Peter
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2009-05-18
- Volume
- 20
- Issue
- 3
- Pages
- 364-376
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2032863178
- Cited by
- 240
- References
- 75
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 9 · 2023: 9 · 2022: 10 · 2021: 11 · 2020: 9 · 2019: 15 · 2018: 8 · 2017: 19 · 2016: 26 · 2015: 18 · 2014: 22 · 2013: 20 · 2012: 20
- FWCI
- 5.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- voluntary wheel running, anxiety-like behavior, adult hippocampal neurogenesis, depression-like behavior, brain-derived neurotrophic factor, corticosterone, stress hormones, emotional behavior, antidepressant effects of exercise, C57BL/6J mice
- MeSH terms
- Doublecortin Domain Proteins, Animals, Anxiety Disorders, Cell Count, Cell Differentiation, Corticosterone, Hippocampus, Male, Mice, Inbred C57BL, Microtubule-Associated Proteins, Neuronal Plasticity, Neuropeptides, Neuropsychological Tests, Physical Conditioning, Animal, Stress, Psychological, Biomarkers, Maze Learning, Brain-Derived Neurotrophic Factor, Ki-67 Antigen, Mice, Neurogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
