Running improves pattern separation during novel object recognition
Open accessAbstract
Running increases adult neurogenesis and improves pattern separation in various memory tasks including context fear conditioning or touch-screen based spatial learning. However, it is unknown whether pattern separation is improved in spontaneous behavior, not emotionally biased by positive or negative reinforcement. Here we investigated the effect of voluntary running on pattern separation during novel object recognition in mice using relatively similar or substantially different objects.We show that running increases hippocampal neurogenesis but does not affect object recognition memory with 1.5 h delay after sample phase. By contrast, at 24 h delay, running significantly improves recognition memory for similar objects, whereas highly different objects can be distinguished by both, running and sedentary mice. These data show that physical exercise improves pattern separation, independent of negative or positive reinforcement. In sedentary mice there is a pronounced temporal gradient for remembering object details. In running mice, however, increased neurogenesis improves hippocampal coding and temporally preserves distinction of novel objects from familiar ones.
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Running induces an increase of performance in different hippocampus-dependent cognitive tasks, such as spatial memory and spatial pattern separation, novel object recognition, and contextual fear conditioning.
“As for running, there is straightforward evidence that, in parallel with the surge of proliferation of progenitor cells, it induces an increase of performance in different hippocampus-dependent cognitive tasks, such as spatial memory and spatial pattern separation (Voss et al., 2013;Creer et al., 2010), or novel object recognition (Bolz et al., 2015) and contextual fear conditioning (Kohman et al.”
From Depression and adult neurogenesis: Positive effects of the antidepressant fluoxetine and of physical exercise (2018) · cites this paper as Bolz et al., 2015
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Cites
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · 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
The Neuroendocrinology of Stress: A Never Ending Story
Lightman, S. L. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01711.x · Cited by 3,570 · 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
Exercise: a behavioral intervention to enhance brain health and plasticity
Cotman, C. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02143-4 · Cited by 2,739 · see citing works
New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?
Deng, W., Aimone, J. B., & Gage, F. H. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2822 · Cited by 2,120 · see citing works
Exercise enhances learning and hippocampal neurogenesis in aged mice
van Praag, H., Shubert, T., Zhao, C., & Gage, F. H. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1731-05.2005 · Cited by 2,078 · see citing works
Functional organization of the hippocampal longitudinal axis
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3785 · Cited by 1,738 · see citing works
A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation
Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., et al. (2009) · Science · doi:10.1126/science.1173215 · Cited by 1,642 · see citing works
Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation
Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011) · Nature · doi:10.1038/nature09817 · Cited by 1,567 · see citing works
Transient expression of doublecortin during adult neurogenesis
Brown, J. P., Couillard‐Després, S., Cooper‐Kuhn, C. M., Winkler, J., Aigner, L., & Kuhn, H. G. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10874 · Cited by 1,494 · see citing works
Internally Generated Cell Assembly Sequences in the Rat Hippocampus
Pastalkova, E., Itskov, V., Amarasingham, A., & Buzsáki, G. (2008) · Science · doi:10.1126/science.1159775 · Cited by 1,301 · see citing works
Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus
Schmidt-Hieber, C., Jonas, P., & Bischofberger, J. (2004) · Nature · doi:10.1038/nature02553 · Cited by 1,292 · see citing works
Self-citationGABA regulates synaptic integration of newly generated neurons in the adult brain
Ge, S., Goh, E. L. K., Sailor, K. A., Kitabatake, Y., Ming, G., & Song, H. (2005) · Nature · doi:10.1038/nature04404 · Cited by 1,261 · see citing works
Requirement for Hippocampal CA3 NMDA Receptors in Associative Memory Recall
Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., Kato, A., Carr, C. A., Johnston, D., Wilson, M. A., et al. (2002) · Science · doi:10.1126/science.1071795 · Cited by 1,090 · see citing works
Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network
McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. (2007) · Science · doi:10.1126/science.1140263 · Cited by 958 · see citing works
A Critical Period for Enhanced Synaptic Plasticity in Newly Generated Neurons of the Adult Brain
Ge, S., Yang, C.-H., Hsu, K.-S., Ming, G.-L., & Song, H. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.002 · Cited by 927 · 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
Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., Barrera, V. R., Chittajallu, R., Iwamoto, K. S., McBain, C. J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.046 · Cited by 805 · see citing works
GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus
Acsády, L., Kamondi, A., Sı́k, A., Freund, T., & Buzsáki, G. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03386.1998 · Cited by 741 · see citing works
TrkB Regulates Hippocampal Neurogenesis and Governs Sensitivity to Antidepressive Treatment
Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C.-H., Kernie, S. G., Bassel-Duby, R., & Parada, L. F. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.023 · Cited by 634 · see citing works
NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus
Tashiro, A., Sandler, V. M., Toni, N., Zhao, C., & Gage, F. H. (2006) · Nature · doi:10.1038/nature05028 · Cited by 620 · see citing works
Effects of Adult Neurogenesis on Synaptic Plasticity in the Rat Dentate Gyrus
Snyder, J. S., Kee, N., & Wojtowicz, J. M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.6.2423 · Cited by 619 · see citing works
Taming anxiety in laboratory mice
Hurst, J. L., & West, R. S. (2010) · Nature Methods · doi:10.1038/nmeth.1500 · Cited by 599 · see citing works
Synapse formation on neurons born in the adult hippocampus
Toni, N., Teng, E. M., Bushong, E. A., Aimone, J. B., Zhao, C., Consiglio, A., van Praag, H., Martone, M. E., Ellisman, M. H., & Gage, F. H. (2007) · Nature Neuroscience · doi:10.1038/nn1908 · Cited by 579 · see citing works
Running enhances spatial pattern separation in mice
Creer, D. J., Romberg, C., Saksida, L. M., van Praag, H., & Bussey, T. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911725107 · Cited by 553 · see citing works
The mechanisms for pattern completion and pattern separation in the hippocampus
Rolls, E. T. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00074 · Cited by 545 · see citing works
Pattern separation: a common function for new neurons in hippocampus and olfactory bulb
Sahay, A., Wilson, D. A., & Hen, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.012 · Cited by 514 · see citing works
Bruel‐Jungerman, E., Laroche, S., & Rampon, C. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03875.x · Cited by 505 · see citing works
Optical controlling reveals time-dependent roles for adult-born dentate granule cells
Gu, Y., Arruda-Carvalho, M., Wang, J., Janoschka, S., Josselyn, S. A., Frankland, P. W., & Ge, S. (2012) · Nature Neuroscience · doi:10.1038/nn.3260 · Cited by 423 · see citing works
Running is the neurogenic and neurotrophic stimulus in environmental enrichment
Kobilo, T., Liu, Q.-R., Gandhi, K., Mughal, M., Shaham, Y., & van Praag, H. (2011) · Learning & Memory · doi:10.1101/lm.2283011 · Cited by 385 · see citing works
Jagasia, R., Steib, K., Englberger, E., Herold, S., Faus-Keßler, T., Saxe, M., Gage, F. H., Song, H., & Lie, D. C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-09.2009 · Cited by 328 · 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
Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel
Czurkó, A., Hirase, H., Csicsvari, J. L., & Buzsáki, G. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00446.x · Cited by 326 · see citing works
Patch-clamp recording from mossy fiber terminals in hippocampal slices
Bischofberger, J., Engel, D., Li, L., Geiger, J. R., & Jónás, P. (2006) · Nature Protocols · doi:10.1038/nprot.2006.312 · Cited by 315 · see citing works
Self-citationTraveling Theta Waves along the Entire Septotemporal Axis of the Hippocampus
Patel, J., Fujisawa, S., Berényi, A., Royer, S., & Buzsáki, G. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.015 · Cited by 306 · see citing works
Adult‐born neurons are necessary for extended contextual discrimination
Tronel, S., Belnoue, L., Grosjean, N., Revest, J., Piazza, P., Koehl, M., & Abrous, D. N. (2010) · Hippocampus · doi:10.1002/hipo.20895 · Cited by 274 · see citing works
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
Redila, V. A., & Christie, B. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.050 · Cited by 235 · see citing works
The Timing for Neuronal Maturation in the Adult Hippocampus Is Modulated by Local Network Activity
Piatti, V. C., Davies-Sala, M. G., Esposito, M. S., Mongiat, L. A., Trinchero, M. F., & Schinder, A. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1380-11.2011 · Cited by 226 · see citing works
Tanti, A., & Belzung, C. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.017 · Cited by 220 · see citing works
Temprana, S. G., Mongiat, L. A., Yang, S. M., Trinchero, M. F., Alvarez, D. D., Kropff, E., Giacomini, D., Beltramone, N., Lanuza, G. M., & Schinder, A. F. (2014) · Neuron · doi:10.1016/j.neuron.2014.11.023 · Cited by 200 · see citing works
Denny, C. A., Burghardt, N. S., Schachter, D., Hen, R., & Drew, M. R. (2011) · Hippocampus · doi:10.1002/hipo.20964 · Cited by 199 · see citing works
Niibori, Y., Yu, T., Epp, J. R., Akers, K. G., Josselyn, S. A., & Frankland, P. W. (2012) · Nature Communications · doi:10.1038/ncomms2261 · Cited by 195 · see citing works
A Critical Period for Experience-Dependent Remodeling of Adult-Born Neuron Connectivity
Bergami, M., Masserdotti, G., Temprana, S. G., Motori, E., Eriksson, T., Göbel, J., Yang, S. M., Conzelmann, K., Schinder, A. F., Götz, M., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.001 · Cited by 191 · see citing works
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
Montero‐Pedrazuela, A., Venero, C., Lavado-Autric, R., Fernández‐Lamo, I., García‐Verdugo, J. M., Bernal, J., & Guadaño‐Ferraz, A. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001802 · Cited by 171 · see citing works
NR2B-Dependent Plasticity of Adult-Born Granule Cells is Necessary for Context Discrimination
Kheirbek, M. A., Tannenholz, L., & Hen, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1692-12.2012 · Cited by 167 · see citing works
Tanti, A., Rainer, Q., Minier, F., Surget, A., & Belzung, C. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.04.022 · Cited by 161 · see citing works
Hopkins, M. E., Nitecki, R., & Bucci, D. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.071 · Cited by 160 · see citing works
Young hippocampal neurons are critical for recent and remote spatial memory in adult mice
Goodman, T. H., Trouche, S. G., Massou, I., Verret, L., Zerwas, M., Roullet, P., & Rampon, C. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.09.047 · Cited by 136 · see citing works
Kitamura, T., Mishina, M., & Sugiyama, H. (2003) · Neuroscience Research · doi:10.1016/s0168-0102(03)00171-8 · Cited by 134 · see citing works
Bechara, R. G., & Kelly, A. M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.02.018 · Cited by 132 · see citing works
Mitochondria Modify Exercise-Induced Development of Stem Cell-Derived Neurons in the Adult Brain
Steib, K., Schäffner, I., Jagasia, R., Ebert, B., & Lie, D. C. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4972-13.2014 · Cited by 128 · see citing works
Jaholkowski, P. P., Kiryk, A., Jedynak, P., Abdallah, N. M. ‐. B., Knapska, E., Kowalczyk, A. E., Piechal, A., Blecharz‐Klin, K., Figiel, I., Lioudyno, V. I., et al. (2009) · Learning & Memory · doi:10.1101/lm.1459709 · Cited by 125 · see citing works
Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network
Bischofberger, J., Engel, D., Frotscher, M., & Jónás, P. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0093-2 · Cited by 117 · see citing works
Self-citationRegulation of hippocampal progenitor cell survival, proliferation and dendritic development by BDNF
Choi, S. H., Li, Y., Parada, L. F., & Sisodia, S. S. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-52 · Cited by 106 · see citing works
Hippocampus‐dependent learning is associated with adult neurogenesis in MRL/MpJ mice
Thuret, S., Toni, N., Aigner, S., Yeo, G. W.-M., & Gage, F. H. (2009) · Hippocampus · doi:10.1002/hipo.20550 · Cited by 79 · see citing works
Babu, H. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.22.001.2009 · Cited by 76 · see citing works
Suárez‐Pereira, I., Canals, S., & Carrión, Á. M. (2014) · Hippocampus · doi:10.1002/hipo.22349 · Cited by 55 · see citing works
The role of the dorsal dentate gyrus in object and object-context recognition
Dees, R. L., & Kesner, R. P. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.07.013 · Cited by 47 · see citing works
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- Authors
- Bolz, L., Heigele, S., & Bischofberger, J.
- Affiliations
- University of Basel (CH)
- Corresponding author
- Bischofberger, Josef
- ORCID
- Bischofberger, Josef
- Venue
- Brain Plasticity
- Publisher
- IOS Press
- Published
- 2015-06
- Volume
- 1
- Issue
- 1
- Pages
- 129-141
- ISSN
- 2213-6304 (ISSN-L)
- 2213-6312
- PMC
- PMC5928530
- OpenAlex
- W1937888283
- Cited by
- 80
- References
- 61
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 5 · 2023: 9 · 2022: 9 · 2021: 13 · 2020: 5 · 2019: 9 · 2018: 7 · 2017: 10 · 2016: 3 · 2015: 2
- FWCI
- 4.41
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Brain Plasticity (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- voluntary running, physical activity, pattern separation, novel object recognition, adult neurogenesis, hippocampus, object recognition memory, memory delay, sedentary mice
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