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The effects of running and of inhibiting adult neurogenesis on learning and memory in rats.
Abstract
The presence of ongoing adult neurogenesis within the highly plastic hippocampal circuitry poses questions as to the relevance of new neurons to learning and memory. Correlational and causal evidence suggests that some, but not all, hippocampal tasks involve the new neurons. The evidence with regard to spatial learning in the water maze, one of the most commonly used hippocampal tasks, is contradictory. In this study we examined the effects of irradiation-induced reduction in neurogenesis on spatial learning and another standard hippocampal task, contextual fear conditioning, in rats that experienced normal cage conditions or voluntary running. The results indicate that reduced neurogenesis had little effect on spatial learning but severely impaired contextual fear conditioning. It was suggested that compensatory mechanisms within the hippocampus may have contributed selectively to sparing of spatial function. Performance on the fear conditioning task was weakly related to enhanced neurogenesis or running. The results improve our understanding of the functional role of adult neurogenesis in behaving animals.
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“For example, inhibiting the rate of cell proliferation in mice was sufficient to impair pattern separation (Deng et al., 2010) and block AE-induced improvements in spatial (Clark et al., 2009) and contextual (Wojtowicz et al., 2008) memory performance, but only in conditions in which the task required fine spatial discriminations (i.e., where pattern separation was necessary; Creer et al., 2010).”
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 Wojtowicz et al., 2008
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Cites
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
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
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
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
Neurogenesis in the adult is involved in the formation of trace memories
Shors, T. J., Miesegaes, G. R., Beylin, A. V., Zhao, M., Rydel, T. A., & Gould, E. (2001) · Nature · doi:10.1038/35066584 · Cited by 2,014
Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. M., & Fuchs, E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02492.1997 · Cited by 1,496
Saxe, M. D., Battaglia, F., Wang, J.-W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D. R., Sofroniew, M. V., Kandel, E. R., Santarelli, L., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607207103 · Cited by 1,020
A role for adult neurogenesis in spatial long-term memory
Snyder, J. S., Hong, N. S., McDonald, R. J., & Wojtowicz, J. M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.10.009 · Cited by 854
Neurogenesis may relate to some but not all types of hippocampal‐dependent learning
Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., & Gould, E. (2002) · Hippocampus · doi:10.1002/hipo.10103 · Cited by 853
Inhibition of neurogenesis interferes with hippocampus‐dependent memory function
Winocur, G., Wojtowicz, J. M., Sekeres, M. J., Snyder, J. S., & Wang, S. Z. (2006) · Hippocampus · doi:10.1002/hipo.20163 · Cited by 601
Olson, A. K., Eadie, B. D., Ernst, C., & Christie, B. R. (2006) · Hippocampus · doi:10.1002/hipo.20157 · Cited by 592
Is there a link between adult neurogenesis and learning?
Leuner, B., Gould, E., & Shors, T. J. (2006) · Hippocampus · doi:10.1002/hipo.20153 · Cited by 543
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
Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment
Meshi, D., Drew, M. R., Saxe, M., Ansorge, M. S., David, D. J. P., Santarelli, L., Malapani, C., Moore, H. M., & Hen, R. (2006) · Nature Neuroscience · doi:10.1038/nn1696 · Cited by 458
Spatial Learning Depends on Both the Addition and Removal of New Hippocampal Neurons
Dupret, D., Fabre, A., Döbrössy, M. D., Panatier, A., Rodriguez, J. J., Lamarque, S., Lemaire, V., Oliet, S. H. R., Piazza, P., & Abrous, D. N. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050214 · Cited by 410
Morris, R. G. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04888.x · Cited by 398
Age-related production of new granule cells in the adult dentate gyrus
Seki, T., & Arai, Y. (1995) · Neuroreport · doi:10.1097/00001756-199512150-00010 · Cited by 386
Tanapat, P., Hastings, N. B., Rydel, T. A., Galea, L. A. M., & Gould, E. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1297 · Cited by 385
Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia.
Zola-Morgan, S. M., & Squire, L. R. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.1.22 · Cited by 367
Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia.
Zola-Morgan, S. M., & Squire, L. R. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.1.22 · Cited by 361
BrdU assay for neurogenesis in rodents
Wojtowicz, J. M., & Kee, N. (2006) · Nature Protocols · doi:10.1038/nprot.2006.224 · Cited by 357
Holmes, G. L. (1990) · Journal of Epilepsy · doi:10.1016/0896-6974(90)90161-q · Cited by 334
Wiskott, L., Rasch, M. J., & Kempermann, G. (2006) · Hippocampus · doi:10.1002/hipo.20167 · Cited by 301
Regulation of Adult Neurogenesis by Psychotropic Drugs and Stress
Duman, R. S., Malberg, J. E., & Nakagawa, S. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29244-2 · Cited by 300
Hippocampal cellular and network activity in freely moving echolocating bats
Ulanovsky, N., & Moss, C. F. (2007) · Nature Neuroscience · doi:10.1038/nn1829 · Cited by 283
Pothuizen, H. H. J., Zhang, W., Jongen‐Rêlo, A. L., Feldon, J., & Yee, B. K. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03170.x · Cited by 274
A computational principle for hippocampal learning and neurogenesis
Becker, S. (2005) · Hippocampus · doi:10.1002/hipo.20095 · Cited by 255
Paradoxical influence of hippocampal neurogenesis on working memory
Saxe, M., Malleret, G., Vronskaya, S., Mendez‐David, I., Garcia, A. D. R., Sofroniew, M. V., Kandel, E. R., & Hen, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611718104 · Cited by 244
Redila, V. A., & Christie, B. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.050 · Cited by 244
Dynamics of neurogenesis in the dentate gyrus of adult rats
Kinkaid, H. Y. M., & Wojtowicz, J. M. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.05.022 · Cited by 228
A model of hippocampal neurogenesis in memory and mood disorders
Becker, S., & Wojtowicz, J. M. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.10.013 · Cited by 211
Winocur, G. (1985) · Behavioural Brain Research · doi:10.1016/0166-4328(85)90088-9 · Cited by 206
Seki, T. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10387 · Cited by 204
Sisti, H. M., Glass, A. L., & Shors, T. J. (2007) · Learning & Memory · doi:10.1101/lm.488707 · Cited by 188
Neurogenesis in a rat model of age‐related cognitive decline
Bizon, J. L., Lee, H. J., & Gallagher, M. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00099.x · Cited by 177
Winocur, G. (1992) · Neuropsychologia · doi:10.1016/0028-3932(92)90081-v · Cited by 155
Impairment of hippocampal neurogenesis in streptozotocin-treated diabetic rats
Zhang, W.-J., Tan, Y., Yue, J. T. Y., Vranić, M., & Wojtowicz, J. M. (2007) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.2007.00928.x · Cited by 150
Naylor, A. S., Persson, A. I., Eriksson, P. S., Jonsdottir, I. H., & Thorlin, T. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01085.2004 · Cited by 127
Absent or Low Rate of Adult Neurogenesis in the Hippocampus of Bats (Chiroptera)
Amrein, I., Dechmann, D. K. N., Winter, Y., & Lipp, H. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000455 · Cited by 126
Learning-Induced Survival of New Neurons Depends on the Cognitive Status of Aged Rats
Drapeau, E., Montaron, M., Aguerre, S., & Abrous, D. N. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1031-07.2007 · Cited by 119
Irradiation as an experimental tool in studies of adult neurogenesis
Wojtowicz, J. M. (2006) · Hippocampus · doi:10.1002/hipo.20158 · Cited by 107
Nadel, L., & Bohbot, V. D. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 92
Dalla, C., Bangasser, D. A., Edgecomb, C., & Shors, T. J. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.02.003 · Cited by 71
Leuner, B., Waddell, J., Gould, E., & Shors, T. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2781-06.2006 · Cited by 60
Cuppini, R., Bucherelli, C., Ambrogini, P., Ciuffoli, S., Orsini, L., Ferri, P., & Baldi, E. (2005) · Hippocampus · doi:10.1002/hipo.20140 · Cited by 30
Do new neurons have a functional role in the adult hippocampus?
Cameron, H. A., & Christie, B. R. (2007) · Debates in Neuroscience · doi:10.1007/s11559-007-9001-y · Cited by 9
Research works printed but not linked: 1
- Shapiro M.L, 1994, Memory Systems., 87
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Sorted by citations
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
The role of adult hippocampal neurogenesis in brain health and disease
Toda, T., Parylak, S. L., Linker, S. B., & Gage, F. H. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0036-2 · Cited by 719
“However, there are a few reports of neurogenesis knockdown impairing the initial acquisition of the Morris water maze [73] or contextual fear conditioning [74, 75], and increasing neurogenesis via running does not universally lead to improvement [76].”
BackgroundJessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D., Consiglio, A., Lie, D. C., Squire, L. R., & Gage, F. H. (2009) · Learning & Memory · doi:10.1101/lm.1172609 · Cited by 654
“For example, classical conditioning of context fear has been reported to be impaired after blocking neurogenesis (Saxe et al. 2006; Winocur et al. 2006; Imayoshi et al. 2008; Wojtowicz et al. 2008 ), whereas contextual fear conditioning has also been reported to be intact after blocking hippocampal neurogenesis (Dupre…”
BackgroundRunning 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
“For example, some researchers found that irradiation of newly born cells in running mice selectively blocked improvement in a general test of hippocampal function, water maze learning (40), but not in contextual fear conditioning (40, 41), whereas others reported opposite findings (42).”
ResultPattern 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
Metadata
- Authors
- Wojtowicz, J. M., Askew, M. L., & Winocur, G.
- Affiliations
- University of Toronto (CA)
- Corresponding author
- Wojtowicz, J. Martin
- ORCID
- Winocur, Gordon
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2008-03
- Volume
- 27
- Issue
- 6
- Pages
- 1494-1502
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2169145097
- Cited by
- 158
- References
- 45
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 4 · 2020: 5 · 2019: 3 · 2018: 1 · 2017: 9 · 2016: 16 · 2015: 15 · 2014: 12 · 2013: 10 · 2012: 10
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Toronto
- National Institutes of Health
- Canadian Institutes of Health Research
- Natural Sciences and Engineering Research Council of Canada
- 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
- adult neurogenesis, voluntary running, hippocampus, spatial learning, contextual fear conditioning, compensatory mechanisms, learning and memory, hippocampal plasticity
- MeSH terms
- Animals, Cell Differentiation, Cobalt Radioisotopes, Fear, Hippocampus, Learning, Male, Memory, Physical Conditioning, Animal, Random Allocation, Rats, Long-Evans, Rats
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