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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Inhibiting the rate of cell proliferation in mice blocked aerobic exercise-induced improvements in contextual memory performance.
“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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A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation
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“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].”
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“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 · see citing works
“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
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“…of neurogenesis impairs contextual fear conditioning (Saxe et al., 2006; Winocur et al., 2006; Imayoshi et al., 2008; WarnerSchmidt et al., 2008; Wojtowicz et al., 2008; HernandezRabaza et al., 2009; Ko et al., 2009), and others reporting no impairment (Shors et al., 2002; Clark et al., 2008;…”
BackgroundResultInfluentialAdult Neurogenesis: Beyond Learning and Memory
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“A recent study by Wojtowicz et al. (2008) examined the effects of running and of inhibiting adult neurogenesis on learning and memory male Long Evans rats, but the rats did not show gains in behavioral performance from exercise on either contextual fear or water maze, so the data are not relevant for evaluating the hy…”
InfluentialNoonan, M. A., Bulin, S. E., Fuller, D. C., & Eisch, A. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4256-09.2010 · Cited by 236 · see citing works
“Based on our study and many others that use similar irradiation paradigms to decrease rat hippocampal neurogenesis (Snyder et al., 2005; Winocur et al., 2006; Wojtowicz and Kee, 2006; Airan et al., 2007; Wojtowicz et al., 2008), this paradigm maintains the integrity of mature hippocampal neurons while ablating neural…”
BackgroundMethodResultInfluentialNeurogenesis-mediated forgetting minimizes proactive interference
Epp, J. R., Mera, R. S., Köhler, S., Josselyn, S. A., & Frankland, P. W. (2016) · Nature Communications · doi:10.1038/ncomms10838 · Cited by 229 · see citing works
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“…in contextual fear conditioning observed after loss of new neurons is consistent with this possibility (Saxe et al., 2006; Winocur et al., 2006; Wojtowicz et al., 2008), as are findings that the ventral, as well as dorsal, hippocampus is important for consolidation of contextual fear memory…”
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“…with cytostatic drugs or irradiation have revealed that the formation of associative memories is altered in some cases (Saxe et al., 2006; Winocur et al., 2006; Wojtowicz et al., 2008; Hernandez-Rabaza et al., 2009) but not in others (Shors et al., 2002; Clark et al., 2008; Kitamura et al., 2009).”
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“For instance, some studies (Farioli-Vecchioli et al., 2008; Imayoshi et al., 2008; Saxe et al., 2006; Warner-Schmidt et al., 2008; Winocur et al., 2006; Wojtowicz et al., 2008; Zhang et al., 2008) trained subjects with pairings between a discrete stimulus and a footshock (a procedure sometimes termed “background” cont…”
InfluentialLithium rescues synaptic plasticity and memory in Down syndrome mice
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“This finding is consistent with previous studies showing that contextual learning (7, 9, 10), spatial memory, and object discrimination (44, 45, 47, 63) rely on hippocampal adult neurogenesis, while working memory engages several brain areas, including the prefrontal cortex, basal forebrain, hippocampus, and striatum…”
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“…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…”
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“…the number of young hippocampal neurons (Mizumatsu et al., 2003; Tada et al., 2000; Wojtowicz, 2006)—causes deficits in long-term retention, but not acquisition, in the Morris water maze (Snyder et al., 2005; Wojtowicz et al., 2008) and spatial working memory in the T-maze (Madsen et al., 2003).”
BackgroundAdult neurogenesis in the mammalian hippocampus: Why the dentate gyrus?Preprint
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“…mice, consistent with network level deficits and the possibility that animals had two overlapping spatial representations active in the DG. Minor deficits in reversal learning in the MWM have also been suggested in animals lacking adult neurogenesis (Wojtowicz et al. 2008; Garthe et al. 2009).”
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“The behavioral tasks used in these studies (8, 21, 23) may not have been sensitive to detecting irradiation-induced deficits.”
InfluentialYoung hippocampal neurons are critical for recent and remote spatial memory in adult mice
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Adult Neurogenesis and the Future of the Rejuvenating Brain Circuits
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SPEAR, L. P. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2013.11.006 · Cited by 116 · see citing works
“These age specific effects are consistent with the impaired context fear retention seen in animals exposed intermittently to EtOH as adolescents but not as adults, given evidence that this hippocampally-dependent task requires formation of new neurons (e.g., Wojtowicz et al, 2008).”
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Helfer, J. L., Goodlett, C. R., Greenough, W. T., & Klintsova, A. Y. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.090 · Cited by 102 · see citing works
“Deficits in spatial working memory and place learning in the Morris water maze have been demonstrated in numerous studies utilizing the postnatal rat model of alcohol exposure (Goodlett and Peterson, 1995; Johnson and Goodlett, 2002; Pauli et al., 1995; Thomas et al., 2008; Wozniak et al., 2004).”
Hernández-Rabaza, V., Hontecillas-Prieto, L., Velázquez-Sánchez, C., Ferragud, A., Pérez-Villaba, A., Arcusa, A., Barcia, J. A., Trejo, J. L., & Canales, J. J. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.06.008 · Cited by 114 · see citing works
Broadwater, M., Liu, W., Crews, F. T., & SPEAR, L. P. (2014) · Developmental Neuroscience · doi:10.1159/000362874 · Cited by 101 · see citing works
“Given that neurogenesis is implicated in context fear retention [11, 12, 13, 14, 15], it is possible that alterations in neurogenesis in the DG as a result of adolescent ethanol exposure may have contributed to deficits in context fear retention previously observed in a separate group of animals [6].”
BackgroundHippocampus-dependent learning influences hippocampal neurogenesis
Epp, J. R., Chow, C., & Galea, L. A. M. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00057 · Cited by 95 · see citing works
“We will not discuss these studies here but they have been reviewed elsewhere (Wojtowicz, 2006; Wojtowicz et al., 2008; Deng et al., 2010).”
MethodJohnston, S. T., Shtrahman, M., Parylak, S., Gonçalves, J. T., & Gage, F. H. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.10.013 · Cited by 98 · see citing works
Current Understanding of the Neural Stem Cell Niches
Llorente, V., Velarde, P., Desco, M., & Gómez‐Gaviro, M. V. (2022) · Cells · doi:10.3390/cells11193002 · Cited by 94 · see citing works
Winocur, G., Wojtowicz, J. M., Huang, J. W., & Tannock, I. F. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3394-0 · Cited by 93 · see citing works
Adult hippocampal neurogenesis and its role in cognition.
Oomen, C. A., Bekinschtein, P., Kent, B. A., Saksida, L. M., & Bussey, T. J. (2014) · WIREs Cognitive Science · doi:10.1002/wcs.1304 · Cited by 93 · see citing works
Juliandi, B., Tanemura, K., Igarashi, K., Tominaga, T., Furukawa, Y., Otsuka, M., Moriyama, N., Ikegami, D., Abematsu, M., Sanosaka, T., et al. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.10.012 · Cited by 87 · see citing works
“…have indicated that ablation of adult neurogenesis in the DG leads to defective performance in a contextual associative test (Saxe et al., 2006; Wojtowicz et al., 2008) (but see Shors et al., 2002), but enhanced neurogenesis or running was weakly related to the performance in the test…”
BackgroundInfluentialHippocampal dysfunctions caused by cranial irradiation: A review of the experimental evidence
Son, Y., Yang, M., Wang, H., & Moon, C. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.01.007 · Cited by 84 · see citing works
“…IR have been investigated, the mediating role of hippocampal neurogenesis is controversial; some researchers argue that it plays a beneficial role (Fan et al., 2007; Ji et al., 2014; Naylor et al., 2008) whereas others suggest it has little effect (Meshi et al., 2006; Wojtowicz et al., 2008).”
BackgroundExercise Regulation of Cognitive Function and Neuroplasticity in the Healthy and Diseased Brain
Hamilton, G. F., & Rhodes, J. S. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.07.004 · Cited by 83 · see citing works
Adult hippocampal neurogenesis and memory interference
Winocur, G., Becker, S., Luu, P., Rosenzweig, S., & Wojtowicz, J. M. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.032 · Cited by 81 · see citing works
“As in a previous study [13], irradiation was admin-”
BackgroundResultLafenêtre, P. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.034.2009 · Cited by 80 · see citing works
Becker, S., MacQUEEN, G. M., & Wojtowicz, J. M. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.095 · Cited by 79 · see citing works
Adult hippocampal neurogenesis of mammals: evolution and life history
Amrein, I., & Lipp, H. (2008) · Biology Letters · doi:10.1098/rsbl.2008.0511 · Cited by 78 · see citing works
Sportiche, N., Suntsova, N., Methippara, M. M., Bashir, T., Mitrani, B., Szymusiak, R. S., & McGinty, D. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.06.038 · Cited by 76 · see citing works
“Some studies failed to find initial acquisition deficits in MWM after suppression of neurogenesis (Shors et al., 2002;Saxe et al., 2006;Raber et al., 2004;Wojtowicz et al., 2008;Jessberger et al., 2009), but deficits may be revealed when more challenging test protocols are used (Zhang et al., 2008).”
BackgroundMethodSchoenfeld, T. J., & Swanson, C. (2021) · Biomolecules · doi:10.3390/biom11081077 · Cited by 78 · see citing works
“Perhaps surprisingly, one of the papers that found effects of irradiation on exercise-enhanced spatial memory failed to find effects on contextual fear conditioning [52], whereas a paper that failed to find spatial memory deficits did see a reduction in contextual fear conditioning following irradiation [54].”
BackgroundShapiro, L. A., Ng, K., Zhou, Q., & Ribak, C. E. (2008) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2008.09.011 · Cited by 75 · see citing works
“Indeed, fear conditioning has been shown to be dependent on newborn neurons in the hippocampus [48,49].”
Mustroph, M. L., Stobaugh, D. J., Miller, D. S., DeYoung, E. K., & Rhodes, J. S. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07828.x · Cited by 74 · see citing works
“Moreover, several papers have provided direct evidence that new neurons can enhance associative learning (Winocur et al., 2006; Wojtowicz et al., 2008; Hernandez-Rabaza et al., 2009; Drew et al., 2010).”
BackgroundBarker, J. M., Boonstra, R., & Wojtowicz, J. M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07823.x · Cited by 72 · see citing works
“…or even improvements, in performance on certain ‘hippocampus-dependent’ tasks after irradiation or genetic ablation of adult neurogenesis in the hippocampus (Shors et al., 2002; Snyder et al., 2005; Leuner et al., 2006; Saxe et al., 2006, 2007; Scharfman & Hen, 2007; Wojtowicz et al., 2008).”
BackgroundKalm, M., Karlsson, N., Nilsson, M. K. L., & Blomgren, K. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.01.006 · Cited by 70 · see citing works
“Morris water maze, fear conditioning and open field (Naylor et al., 2008; Raber et al., 2011; Rola et al., 2004; Wojtowicz et al., 2008).”
Namba, T., Ming, G., Song, H., Waga, C., Enomoto, A., Kaibuchi, K., Kohsaka, S., & Uchino, S. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07282.x · Cited by 70 · see citing works
Clark, P., Bhattacharya, T. K., Miller, D. S., & Rhodes, J. S. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.072 · Cited by 71 · see citing works
“Recent studies using irradiation to reduce neurogenesis from running did not report any impairments in wheel running or motor task performance, so new neurons may not be critical for sensory or motor processing (Clark et al., 2008; Wojtowicz et al., 2008).”
Functional and mechanistic exploration of an adult neurogenesis‐promoting small molecule
Petřík, D., Jiang, Y., Birnbaum, S. G., Powell, C. M., Kim, M., Hsieh, J., & Eisch, A. J. (2012) · The FASEB Journal · doi:10.1096/fj.11-201426 · Cited by 68 · see citing works
When is adult hippocampal neurogenesis necessary for learning? Evidence from animal research
Castilla‐Ortega, E., Pedraza, C., Estivill‐Torrús, G., & Santín, L. J. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.027 · Cited by 66 · see citing works
“…that achieved a better performance also possessed more new hippocampal neurons [water maze (Ambrogini et al. , 2000 ; Drapeau et al. , 2003 ; Sisti et al. , 2007 ), contextual fear conditioning (Wojtowicz et al. , 2008 ) and trace conditioning (Leuner et al. , 2004 ; Dalla et al. , 2007 , 2009 )].”
BackgroundInfluentialTime-dependent involvement of adult-born dentate granule cells in behavior
Kim, W. R., Christian, K. M., Ming, G., & Song, H. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.07.012 · Cited by 65 · see citing works
The Ever-Changing Morphology of Hippocampal Granule Neurons in Physiology and Pathology
Llorens-Martı́n, M., Rábano, A., & Ávila, J. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00526 · Cited by 61 · see citing works
“Furthermore, such exposure impairs hippocampal-dependent learning (Wojtowicz et al., 2008; Hernandez-Rabaza et al., 2009).”
Central Nervous System Effects of Whole-Body Proton Irradiation
Sweet, T. B., Panda, N., Hein, A. M., Das, S. L., Hurley, S. D., Olschowka, J. A., Williams, J. P., & O’Banion, M. K. (2014) · Radiation Research · doi:10.1667/rr13699.1 · Cited by 64 · see citing works
Clark, P., Bhattacharya, T. K., Miller, D. S., Kohman, R. A., DeYoung, E. K., & Rhodes, J. S. (2012) · Hippocampus · doi:10.1002/hipo.22020 · Cited by 53 · see citing works
“Literature directly assessing the contribution of exerciseinduced neurogenesis to cognitive performance is scarce (Wojtowicz et al., 2008; Wong-Goodrich et al., 2010; Winocur et al., 2011).”
BackgroundBarlind, A., Karlsson, N., Björk‐Eriksson, T., Isgaard, J., & Blomgren, K. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-2095-8 · Cited by 49 · see citing works
“This might oVer an explanation to why mice generally perform less consistently than rats in active avoidance test protocols such as the MWM. Mice are known to perform more consistently in exploration-based memory tests, for example (D’Hooge and De Deyn 2001).”
BackgroundInfluentialNuclear deterrents: Intrinsic regulators of IL-1β-induced effects on hippocampal neurogenesis
Ó’Léime, C. S., Cryan, J. F., & Nolan, Y. M. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.07.153 · 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
Trivedi, M. H., Greer, T. L., Grannemann, B. D., Church, T. S., Somoza, E. C., Blair, S. N., Szapocznik, J., Stoutenberg, M., Rethorst, C. D., Warden, D., et al. (2011) · Trials · doi:10.1186/1745-6215-12-206 · Cited by 49 · see citing works
“Similar results have been found for exercise-induced hippocampal neurogenesis and improvements in spatial memory in rats and mice [33-35].”
ResultSynaptogenesis in adult‐generated hippocampal granule cells is affected by behavioral experiences
Ambrogini, P., Cuppini, R., Lattanzi, D., Ciuffoli, S., Frontini, A., & Fanelli, M. (2009) · Hippocampus · doi:10.1002/hipo.20679 · Cited by 48 · see citing works
“Adult neurogenesis is involved in some kinds of hippocampus-dependent learning (Shors et al., 2001, 2002; Madsen et al., 2003; Winocur et al., 2006; Wojtowicz et al., 2008).”
BackgroundNeurogenesis, Exercise, and Cognitive Late Effects of Pediatric Radiotherapy
Rodgers, S. P., Treviño, M., Zawaski, J. A., Gaber, M. W., & Leasure, J. L. (2013) · Neural Plasticity · doi:10.1155/2013/698528 · Cited by 47 · see citing works
Merritt, J. R., & Rhodes, J. S. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.11.030 · Cited by 46 · see citing works
Targeting Adult Neurogenesis to Optimize Hippocampal Circuits in Aging
McAvoy, K. M., & Sahay, A. (2017) · Neurotherapeutics · doi:10.1007/s13311-017-0539-6 · Cited by 44 · see citing works
“Studies using the MWM have found that ablation of adult-born DGCs impairs spatial memory only when the target location of the hidden platform is reversed [143, 144].”
BackgroundNamba, T., Maekawa, M., Yuasa, S., Kohsaka, S., & Uchino, S. (2008) · Glia · doi:10.1002/glia.20831 · Cited by 45 · see citing works
“, 2004) and cognitive functions, including learning and memory (Becker and Wojtowicz, 2007; Kee et al., 2007; Wojtowicz et al., 2008).”
BackgroundCanales, J. J. (2010) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32833e16b6 · Cited by 41 · see citing works
“Similarly, irradiation in rats had no effects on spatial learning (Wojtowicz et al., 2008).”
BackgroundVoluntary wheel running enhances contextual but not trace fear conditioning
Kohman, R. A., Clark, P., DeYoung, E. K., Bhattacharya, T. K., Venghaus, C. E., & Rhodes, J. S. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.031 · Cited by 40 · see citing works
Bhattacharya, T. K., Pence, B. D., Ossyra, J. M., Gibbons, T. E., Perez, S., McCusker, R. H., Kelley, K. W., Johnson, R. W., Woods, J. A., & Rhodes, J. S. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.03.023 · Cited by 40 · see citing works
“While exercise improves behavioral performance across multiple domains of cognition, one of the most robust effects of exercise on any hippocampal-involved behavioral measure is contextual fear conditioning [22,24–26].”
Transgenic mouse models for studying adult neurogenesis
Semerci, F., & Maletić‐Savatić, M. (2016) · Frontiers in Biology · doi:10.1007/s11515-016-1405-3 · Cited by 42 · see citing works
Neural Activity Patterns Underlying Spatial Coding in the Hippocampus
Sosa, M., Gillespie, A. K., & Frank, L. M. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_462 · Cited by 39 · see citing works
“The regular addition of new neurons to DG circuitry has major implications for network activity in the region (Ge et al. 2008; Schmidt-Hieber et al. 2004) and for behavior dependent on the DG (Dupret et al. 2008; Garthe et al. 2009; Jessberger et al. 2009; Shors et al. 2001; Wojtowicz et al. 2008).”
BackgroundKlaus, F., & Amrein, I. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.027 · Cited by 40 · see citing works
Hu, P., Wang, Y., Liu, J., Meng, F., Qi, X., Chen, L., van Dam, A., Joëls, M., Lucassen, P. J., & Zhou, J. (2016) · Hippocampus · doi:10.1002/hipo.22574 · Cited by 39 · see citing works
“In humans, accutane is a comparable compound and its oral doses of 0.5– 2.0 mg/kg per day were also linked to depressive symptoms before (Hazen et al., 1983; Wysowski et al., 2001; Bremner et al., 2012).”
BackgroundInfluentialKarlsson, N., Kalm, M., Nilsson, M. K. L., Mallard, C. E., Björk‐Eriksson, T., & Blomgren, K. (2010) · Radiation Research · doi:10.1667/rr2231.1 · Cited by 38 · see citing works
Neurogenesis and pattern separation: time for a divorce
Becker, S. (2016) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1427 · Cited by 35 · see citing works
Deficient plasticity in the hippocampus and the spiral of addiction: focus on adult neurogenesis.
Canales, J. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_230 · Cited by 35 · see citing works
“2006), and irradiation in rats had no effect on spatial learning (Wojtowicz et al. 2008).”
BackgroundCapilla‐González, V., Gil‐Perotín, S., Ferragud, A., Bonet‐Ponce, L., Canales, J. J., & García‐Verdugo, J. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029891 · Cited by 34 · see citing works
“Morris Water Maze [55,56], and T-Maze tasks [57].”
MethodThe future of cognitive neurorehabilitation
Stuss, D. T. (2011) · Neuropsychological Rehabilitation · doi:10.1080/09602011.2011.605590 · Cited by 34 · see citing works
Adult neurogenesis mediates forgetting of multiple types of memory in the rat
Scott, G. A., Terstege, D. J., Roebuck, A. J., Gorzo, K. A., Vu, A. P., Howland, J. G., & Epp, J. R. (2021) · Molecular Brain · doi:10.1186/s13041-021-00808-4 · Cited by 33 · see citing works
“Neurogenesis was substantially increased by voluntary exercise, replicating a large body of previous findings [4, 7, 8, 12, 18, 19, 23].”
MethodResultInfluentialTranslating the impact of exercise on cognition: Methodological issues in animal research
Hatchard, T., Ting, J., & Messier, C. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.06.043 · Cited by 33 · see citing works
Factors affecting graded and ungraded memory loss following hippocampal lesions.
Winocur, G., Moscovitch, M., & Sekeres, M. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.10.001 · Cited by 26 · see citing works
Benice, T. S., & Raber, J. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.028 · Cited by 31 · see citing works
“, 2006), but not all (Wojtowicz et al., 2008), using irradiation to suppress new neuron production have reported disruption in spatial learning and memory in the reference memory version of the Morris water maze.”
BackgroundKida, E., Rabe, A., Walus, M., Albertini, G., & Golabek, A. A. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.11.022 · Cited by 30 · see citing works
“, 2003); reduction in neurogenesis by irradiation had little effect on the spatial learning in rats (Wojtowicz et al., 2008); and running improved the performance of Ts65Dn mice in the Morris water maze, but did not rescue altered neurogenesis in these animals (Llorens-Martín et al.”
BackgroundHippocampal neurogenesis in food‐storing red squirrels: the impact of age and spatial behavior
Johnson, K. M., Boonstra, R., & Wojtowicz, J. (2010) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2010.00589.x · Cited by 3 · see citing works
“Detailed laboratory studies provide support for subtle contribution of new neurons in flexible learning strategies and in contextual learning (Garthe et al. 2009; Wojtowicz et al. 2008).”
Loxton, D., & Canales, J. J. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.11.003 · Cited by 29 · see citing works
“This is consistent with the observation that inhibition of adult hippocampal neurogenesis does not generally impact on this type of memory (Hernandez-Rabaza et al., 2009, Wojtowicz et al., 2008), except when the long-term retention of a spatial location is required (Jessberger et al., 2009).”
Déry, N., Goldstein, A., & Becker, S. (2015) · Behavioral Neuroscience · doi:10.1037/bne0000073 · Cited by 28 · see citing works
Lazic, S. E. (2011) · Journal of The Royal Society Interface · doi:10.1098/rsif.2011.0510 · Cited by 27 · see citing works
Girbovan, C., Kent, P., Merali, Z., & Plamondon, H. (2015) · Nutritional Neuroscience · doi:10.1179/1476830515y.0000000020 · Cited by 27 · 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
Cyclin D2 knockout mice with depleted adult neurogenesis learn Barnes maze task.
Urbach, A., Robakiewicz, I., Baum, E., Kaczmarek, L., Witte, O. W., & Filipkowski, R. K. (2012) · Behavioral Neuroscience · doi:10.1037/a0031222 · Cited by 24 · see citing works
Regulation of behaviour by the nuclear receptor TLX
O'Leary, J. D., O'Leary, O., Cryan, J., & Nolan, Y. (2018) · Genes, Brain and Behavior · doi:10.1111/gbb.12357 · Cited by 22 · see citing works
“It should be noted however that controversy remains regarding the role of adult hippocampal neurogenesis in spatial learning (Arruda-Carvalho et al. 2011; Ben Abdallah et al. 2013; Clelland et al. 2009; Drapeau et al. 2003; Saxe et al. 2006; Snyder et al. 2005; Wojtowicz et al. 2008).”
Background
- 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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