Cited by 755Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanisms

The DOI matches its Crossref record; 42 of the 42 references it cites were found in a registry or an index.

Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice

Rampon, Claire, Tang, Ya-Ping, Goodhouse, Joe, Shimizu, Eiji, Kyin, Maureen, Tsien, Joe Z.·2000·Nature Neuroscience

DOI 10.1038/72945

Open this paper in CoChat — free account

Abstract

We produced CA1-specific NMDA receptor 1 subunit-knockout (CA1-KO) mice to determine the NMDA receptor dependence of nonspatial memory formation and of experience-induced structural plasticity in the CA1 region. CA1-KO mice were profoundly impaired in object recognition, olfactory discrimination and contextual fear memories. Surprisingly, these deficits could be rescued by enriching experience. Using stereological electron microscopy, we found that enrichment induced an increase of the synapse density in the CA1 region in knockouts as well as control littermates. Therefore, our data indicate that CA1 NMDA receptor activity is critical in hippocampus-dependent nonspatial memory, but is not essential for experience-induced synaptic structural changes.

Integrity signals

Registry

Crossref · 10.1038/72945

Cites

42 of 42 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376
More hippocampal neurons in adult mice living in an enriched environment
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997) · Nature · doi:10.1038/386493a0 · Cited by 3,586
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292
mouse brain in stereotaxic coordinates
Franklin, K. B. J., & Paxinos, G. (1997) · Cited by 3,258
The unbiased estimation of number and sizes of arbitrary particles using the disector
Sterio, D. C. (1984) · Journal of Microscopy · doi:10.1111/j.1365-2818.1984.tb02501.x · Cited by 2,533
Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus
Zola-Morgan, S., Squire, L., & Amaral, D. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02950.1986 · Cited by 1,997
Genetic enhancement of learning and memory in mice
Tang, Y., Shimizu, E., Dubé, G., Rampon, C., Kerchner, G. A., Zhuo, M., Liu, G., & Tsien, J. Z. (1999) · Nature · doi:10.1038/43432 · Cited by 1,878
Self-citation
The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782
Self-citation

Flagged first, then by citations

Show all 41 references

Research works printed but not linked: 2

Greenough, W. T., Withers, G. S. & Wallace, C. S. in The Biology of Memory (eds. Squire, L. R. & Lindenbaum, E.) 159–185 (Schattauer, Stuttgart, 1990).
Gray, E. G. Axosomatic and axodendritic synapses of the cerebral cortex: An electron microscopic study. J. Anat. 83, 420– 433 (1959).

Sorted by citations

Items 301–400 of 734

Exercise Paradigms to Study Brain Injury Recovery in Rodents
Arida, R. M., Scorza, F. A., da Silva, S. G., Cysneiros, R. M., & Cavalheiro, É. A. (2011) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0b013e3182063a9c · Cited by 57
Environmental Enrichment Rescues Postnatal Neurogenesis Defect in the Male and Female Ts65Dn Mouse Model of Down Syndrome
Chakrabarti, L., Scafidi, J., Gallo, V., & Haydar, T. F. (2011) · Developmental Neuroscience · doi:10.1159/000329423 · Cited by 57
Role of apolipoprotein E in anxiety
Raber, J. (2007) · Neural Plasticity · doi:10.1155/2007/91236 · Cited by 44
Hippocampal Formation Lesions Impair Performance in an Odor-Odor Association Task Independently of Spatial Context
Alvarez, P. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4068 · Cited by 57
Changes in expression of NMDA-NR1 receptor subunits in the rostral ventromedial medulla modulate pain behaviors
da Silva, L. F. S., Walder, R. Y., Davidson, B. L., Wilson, S. P., & Sluka, K. A. (2010) · Pain · doi:10.1016/j.pain.2010.06.037 · Cited by 56
Distinct gene expression profiles in hippocampus and amygdala after fear conditioning
Mei, B., Li, C., Dong, S., Jiang, C. H., Wang, H., & Hu, Y. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.03.023 · Cited by 56
Modulation of synaptic plasticity and Tau phosphorylation by wild-type and mutant presenilin1
Dewachter, I., Ris, L., Croes, S., Borghgraef, P., Devijver, H., Voets, T., Nilius, B., Godaux, E., & LEUVEN, F. V. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.11.019 · Cited by 56
OLMα2 Cells Bidirectionally Modulate Learning
Siwani, S., França, A. S. C., Mikulovic, S., Reis, A., Hilscher, M. M., Edwards, S. J., Leão, R. N., Tort, A. B. L., & Kullander, K. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.022 · Cited by 59
Is exposure to enriched environment beneficial for functional post-lesional recovery in temporal lobe epilepsy?
Dhanushkodi, A., & Shetty, A. K. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.10.004 · Cited by 55
RNA interference in hippocampus demonstrates opposing roles for CREB and PP1α in contextual and temporal long‐term memory
Peters, M., Bletsch, M., Catapano, R., Zhang, X., Tully, T., & Bourtchouladze, R. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00474.x · Cited by 57
Chronic stress and a cyclic regimen of estradiol administration separately facilitate spatial memory: Relationship with hippocampal CA1 spine density and dendritic complexity.
Conrad, C. D., McLaughlin, K. J., Huynh, T. N., El-Ashmawy, M., & Sparks, M. (2011) · Behavioral Neuroscience · doi:10.1037/a0025770 · Cited by 55
Extracellular diffusion is fast and isotropic in the stratum radiatum of hippocampal CA1 region in rat brain slices
Hrabetova, S. (2005) · Hippocampus · doi:10.1002/hipo.20068 · Cited by 52
Three laws of branding: Neuroscientific foundations of effective brand building
Walvis, T. (2007) · Journal of Brand Management · doi:10.1057/palgrave.bm.2550139 · Cited by 60
Neonatal exposure to novelty enhances long‐term potentiation in CA1 of the rat hippocampus
Tang, A. C., & Zou, B. (2002) · Hippocampus · doi:10.1002/hipo.10017 · Cited by 56
Reversion of age-related recognition memory impairment by iron chelation in rats
de Lima, M. N. M., Dias, C. P., Torres, J. P., Dornelles, A. D. S., Garcia, V. A., Scalco, F. S., Guimarães, M. R., Petry, R. C., Bromberg, E., Constantino, L. D. S., et al. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.02.006 · Cited by 55
Enriched housing reverses age-associated impairment of cognitive functions and tPA-dependent maturation of BDNF
Obiang, P., Maubert, E., Bardou, I., Nicole, O., Launay, S., Bezin, L., Vivien, D., & Agin, V. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.03.004 · Cited by 65
Progressive Age-Related Cognitive Decline in Tau Mice
der Jeugd, A. V., Vermaercke, B., Derisbourg, M. J., Lo, A. C., Hamdane, M., Blum, D. L., Buée, L., & D’Hooge, R. (2013) · Journal of Alzheimer s Disease · doi:10.3233/jad-130110 · Cited by 66
Modeling Brain Reserve: Experience-Dependent Neuronal Plasticity in Healthy and Huntington's Disease Transgenic Mice
Nithianantharajah, J., Barkus, C., Vijiaratnam, N., Clément, O., & Hannan, A. J. (2009) · American Journal of Geriatric Psychiatry · doi:10.1097/jgp.0b013e318196a632 · Cited by 54
Testing experience and environmental enrichment potentiated open-field habituation and grooming behaviour in rats
Rojas‐Carvajal, M., Fornaguera, J., Mora-Gallegos, A., & Brenes, J. C. (2018) · Animal Behaviour · doi:10.1016/j.anbehav.2018.01.018 · Cited by 59
Environmental change during postnatal development alters behaviour, cognitions and neurogenesis of mice
Iso, H., Shimoda, S., & Matsuyama, T. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.01.025 · Cited by 52
Single enrichment variables differentially reduce age-related memory decline in female mice.
Harburger, L. L., Nzerem, C. K., & Frick, K. M. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.4.679 · Cited by 56
Environmental enrichment: Evidence for an unexpected therapeutic influence
Kotloski, R. J., & Sutula, T. P. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.11.012 · Cited by 54
Diphenyl ditelluride impairs short-term memory and alters neurochemical parameters in young rats
Stangherlin, E. C., da Rocha, J. B. T., & Nogueira, C. W. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.08.020 · Cited by 52
Involvement of NMDA receptors in both MPTP-induced neuroinflammation and deficits in episodic-like memory in Wistar rats
Wang, A., Liou, Y., Pawlak, C. R., & Ho, Y. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.11.006 · Cited by 52
The Environment versus Genetics in Controlling the Contribution of MAP Kinases to Synaptic Plasticity
Li, S., Tian, X., Hartley, D. M., & Feig, L. A. (2006) · Current Biology · doi:10.1016/j.cub.2006.10.028 · Cited by 52
Environmental enrichment during adolescence regulates gene expression in the striatum of mice
Thiriet, N., Amar, L., Toussay, X., Lardeux, V., Ladenheim, B., Becker, K. G., Cadet, J. L., Solinas, M., & Jaber, M. (2008) · Brain Research · doi:10.1016/j.brainres.2008.05.030 · Cited by 51
MHC class I immune proteins are critical for hippocampus-dependent memory and gate NMDAR-dependent hippocampal long-term depression
Nelson, P. A., Sage, J. R., Wood, S. C., Davenport, C. M., Anagnostaras, S. G., & Boulanger, L. M. (2013) · Learning & Memory · doi:10.1101/lm.031351.113 · Cited by 49
“Object recognition learning is a second form of hippocampus- and NMDAR-dependent learning that has been examined extensively in humans, monkeys, and rodents (Rampon et al. 2000; Broadbent et al. 2010).”
Background
Knocking‐down the NMDAR1 subunit in a limited amount of neurons in the rat hippocampus impairs learning
Cheli, V. T., Adrover, M. F., Blanco, C., Ferrari, C. C., Cornea, A. M., Pitossi, F. J., Epstein, A. L., & Jerusalinsky, D. A. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03592.x · Cited by 51
Fragile X mental retardation protein levels increase following complex environment exposure in rat brain regions undergoing active synaptogenesis
Irwin, S. A., Christmon, C. A., Grossman, A. W., Galvez, R., Kim, S. H., DeGrush, B. J., Weiler, I. J., & Greenough, W. T. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.11.004 · Cited by 51
On the epigenetic evolution of species-specific perception: The developmental manifold concept
Gottlieb, G. (2002) · Cognitive Development · doi:10.1016/s0885-2014(02)00120-x · Cited by 85
Differential neuronal plasticity in mouse hippocampus associated with various periods of enriched environment during postnatal development
Hosseiny, S., Piétri, M., Petit-Paitel, A., Zarif, H., Heurteaux, C., Chabry, J., & Guyon, A. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0865-y · Cited by 50
Animal models of mental retardation: from gene to cognitive function
Branchi, I., Bichler, Z., Berger-Sweeney, J. E., & Ricceri, L. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00016-2 · Cited by 52
Endophenotypes in normal brain morphology and Alzheimer's disease: a review
Reitz, C., & Mayeux, R. P. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.04.006 · Cited by 53
Modulation of NR2B-regulated contextual fear in the hippocampus by the tissue plasminogen activator system
Norris, E. H., & Strickland, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705848104 · Cited by 49
Impact of IVC housing on emotionality and fear learning in male C3HeB/FeJ and C57BL/6J mice
Kallnik, M., Elvert, R., Ehrhardt, N., Kissling, D., Mahabir, E., Welzl, G., Faus-Kessler, T., de Angelis, M. H., Wurst, W., Schmidt, J., et al. (2007) · Mammalian Genome · doi:10.1007/s00335-007-9002-z · Cited by 58
Visual perception and memory systems: from cortex to medial temporal lobe
Khan, Z. U., Martín‐Montañez, E., & Baxter, M. G. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0641-6 · Cited by 53
Use It or Lose It: Environmental Enrichment as a Means to Promote Successful Cognitive Aging
Frick, K. M., & Benoit, J. D. (2010) · The Scientific World JOURNAL · doi:10.1100/tsw.2010.111 · Cited by 51
Brief environmental enrichment elicits metaplasticity of hippocampal synaptic potentiation in vivo
Buschler, A., & Manahan‐Vaughan, D. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00085 · Cited by 48
The search for a hippocampal engram
Mayford, M. R. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0161 · Cited by 51
Prefrontal Cortex-Mediated Impairments in a Genetic Model of NMDA Receptor Hypofunction Are Reversed by the Novel M1PAM VU6004256
Grannan, M. D., Mielnik, C. A., Moran, S. P., Gould, R. W., Ball, J., Lu, Z., Bubser, M., Ramsey, A. J., Abe, M., Cho, H. P., et al. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00230 · Cited by 51
Assessments of Cognitive Deficits in Mutant Mice
Levin, E. D., & Buccafusco, J. J. (2006) · CRC Press eBooks · doi:10.1201/9781420004335-17 · Cited by 48
DNA Modifications and Neurological Disorders
Weng, Y., An, R., Shin, J., Song, H., & Ming, G. (2013) · Neurotherapeutics · doi:10.1007/s13311-013-0223-4 · Cited by 49
Environmental Enrichment Enhances Episodic-Like Memory in Association with a Modified Neuronal Activation Profile in Adult Mice
Léger, M., Quiedeville, A., Païzanis, E., Natkunarajah, S., Fréret, T., Boulouard, M., & Schumann‐Bard, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048043 · Cited by 51
Handling and environmental enrichment do not rescue learning and memory impairments in αCamKIIT286A mutant mice
Need, A. C., & Giese, K.-P. (2003) · Genes Brain & Behavior · doi:10.1034/j.1601-183x.2003.00020.x · Cited by 47
Hippocampal Synaptic Modulation by the Phosphotyrosine Adapter Protein ShcC/N-Shc via Interaction with the NMDA Receptor
Miyamoto, Y., Chen, L., Sato, M., Sokabe, M., Nabeshima, T., Pawson, T. J., Sakai, R., & Mori, N. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3030-04.2005 · Cited by 47
Effects of β-carboline alkaloids on the object recognition task in mice
Moura, D. J., Rorig, C., Vieira, D. L., Henriques, J. A. P., Roesler, R., Saffi, J., & Boeira, J. M. (2006) · Life Sciences · doi:10.1016/j.lfs.2006.07.004 · Cited by 47
Novel object recognition ability in female mice following exposure to nanoparticle-rich diesel exhaust
Win‐Shwe, T., Fujimaki, H., Fujitani, Y., & Hirano, S. (2012) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2012.05.015 · Cited by 47
Multi-input Synapses, but Not LTP-Strengthened Synapses, Correlate with Hippocampal Memory Storage in Aged Mice
Aziz, W., Kraev, I., Mizuno, K., Kirby, A. J., Fang, T., Rupawala, H., Kasbi, K., Rothe, S., Jozsa, F., Rosenblum, K., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.064 · Cited by 45
Prenatal and Early‐Life Exposure to High‐Level Diesel Exhaust Particles Leads to Increased Locomotor Activity and Repetitive Behaviors in Mice
Rajamani, K. T., Doherty-Lyons, S., Bolden, C. A., Willis, D., Hoffman, C. A., Zelikoff, J. T., Chen, L., & Gu, H. H. (2013) · Autism Research · doi:10.1002/aur.1287 · Cited by 46
Short-term environmental enrichment decreases the mnemonic response to estrogen in young, but not aged, female mice.
Gresack, J., Kerr, K. M., & Frick, K. (2007) · Brain Research · doi:10.1016/j.brainres.2007.05.033 · Cited by 50
A simple webcam-based approach for the measurement of rodent locomotion and other behavioural parameters
Tort, A. B. L., Neto, W. P., Amaral, O. B., Kazlauckas, V., Souza, D. O., & Lara, D. R. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.04.005 · Cited by 46
Environment enrichment rescues the neurodegenerative phenotypes in presenilins‐deficient mice
Dong, S., Li, C., Wu, P., Tsien, J. Z., & Hu, Y. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05641.x · Cited by 46
Self-citation
Use it and boost it with physical and mental activity.
Korol, D. L., Gold, P. E., & Scavuzzo, C. J. (2013) · Hippocampus · doi:10.1002/hipo.22197 · Cited by 45
“…generalize broadly, such as enriched environments benefiting many functions including object recognition, cued and contextual conditioning, spatial learning, and motor ability (Greenough et al., 1972; Kolb and Gibb, 1991; Rampon et al., 2000; Dishman et al., 2006; Frick and Benoit, 2010).”
Background
n-3 PUFA status affects expression of genes involved in neuroenergetics differently in the fronto-parietal cortex compared to the CA1 area of the hippocampus: effect of rest and neuronal activation in the rat.
Harbeby, E., Jouin, M., Alessandri, J., Lallemand, M.-S., Linard, A., Lavialle, M., Huertas, A., Cunnane, S., & Guesnet, P. (2012) · Prostaglandins, Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2012.04.008 · Cited by 43
Sex-specific strategies in spatial orientation in C57BL/6J mice
Bettis, T. J., & Jacobs, L. F. (2009) · Behavioural Processes · doi:10.1016/j.beproc.2009.07.004 · Cited by 43
Excitatory Amino Acid Neurotransmission
Zieglgänsberger, W., Parsons, C. G., & Danysz, W. (2005) · Springer eBooks · doi:10.1007/3-540-28082-0_10 · Cited by 47
Effect of 1.8 GHz radiofrequency electromagnetic radiation on novel object associative recognition memory in mice
Wang, K., Lü, J., Xing, Z.-H., Zhao, Q., Hu, L.-Q., Xue, L., Zhang, J., & Mei, Y. (2017) · Scientific Reports · doi:10.1038/srep44521 · Cited by 46
Dynamic and stable hippocampal representations of social identity and reward expectation support associative social memory in male mice
Kong, E., Lee, K.-H., Do, J., Kim, P., & Lee, D. (2023) · Nature Communications · doi:10.1038/s41467-023-38338-3 · Cited by 48
Early Structural and Functional Defects in Synapses and Myelinated Axons in Stratum Lacunosum Moleculare in Two Preclinical Models for Tauopathy
Maurin, H., Chong, S., Kraev, I., Davies, H. A., Kremer, A., Seymour, C. M., Lechat, B., Jaworski, T., Borghgraef, P., Devijver, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087605 · Cited by 44
Paradoxical Facilitatory Effect of Low-Dose Alcohol Consumption on Memory Mediated by NMDA Receptors
Kalev‐Zylinska, M. L., & During, M. J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2789-07.2007 · Cited by 45
Enhanced recognition memory following glycine transporter 1 deletion in forebrain neurons.
Singer, P., Boison, D., Möhler, H., Feldon, J., & Yee, B. K. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.5.815 · Cited by 44
Short-Term Enrichment Makes Male Rats More Attractive, More Defensive and Alters Hypothalamic Neurons
Mitra, R., & Sapolsky, R. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036092 · Cited by 42
Neuritin reverses deficits in murine novel object associative recognition memory caused by exposure to extremely low-frequency (50 Hz) electromagnetic fields
Zhao, Q., Lü, J., Yao, J., Zhang, Z., Ling, C., & Mei, Y. (2015) · Scientific Reports · doi:10.1038/srep11768 · Cited by 46
Role of H3-Receptor-Mediated Signaling in Anxiety and Cognition in Wild-Type and Apoe–/– Mice
Bongers, G., Leurs, R., Robertson, J., & Raber, J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300352 · Cited by 43
Experience-Dependent, Rapid Structural Changes in Hippocampal Pyramidal Cell Spines
Kitanishi, T., Ikegaya, Y., Matsuki, N., & Yamada, M. K. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp012 · Cited by 42
A Genetic Neuroscience Approach to Human Cognition
de Geus, E. J. C., & Boomsma, D. I. (2001) · European Psychologist · doi:10.1027//1016-9040.6.4.241 · Cited by 43
Environmental enrichment increases amphetamine-induced glutamate neurotransmission in the nucleus accumbens: A neurochemical study
Rahman, S., & Bardo, M. T. (2008) · Brain Research · doi:10.1016/j.brainres.2007.12.052 · Cited by 42
Memantine prevents the cognitive impairment induced by 3,4-methylenedioxymethamphetamine in rats
Camarasa, J., Marimón, J. M., Rodrigo, T., Escubedo, E., & Pubill, D. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.05.014 · Cited by 42
Enrichment-induced exercise to quantify the effect of different housing conditions: A tool to standardize enriched environment protocols
Xie, H., Wu, Y., Jia, J., Liu, G., Zhang, Q., Yu, K., Guo, Z., Shen, L. W., & Hu, R. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.032 · Cited by 42
The effect of NMDA-NR2B receptor subunit over-expression on olfactory memory task performance in the mouse
White, T. L., & Youngentob, S. L. (2004) · Brain Research · doi:10.1016/j.brainres.2004.05.114 · Cited by 42
Growth hormone and IGF-I modulate local cerebral glucose utilization and ATP levels in a model of adult-onset growth hormone deficiency
Sonntag, W. E., Bennett, C., Ingram, R. L., Donahue, A., Ingraham, J., Chen, H., Moore, T., Brunso‐Bechtold, J. K., & Riddle, D. R. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00012.2006 · Cited by 42
Biological Psychology
Clark, R. E., Hales, J. B., Zola, S. M., & Thompson, R. F. (2012) · Wiley eBooks · doi:10.1002/9781118133880.hop201005 · Cited by 42
Genetic Overexpression of NR2B Subunit Enhances Social Recognition Memory for Different Strains and Species
Jacobs, S., & Tsien, J. Z. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036387 · Cited by 40
Self-citation
Neurological characterization of mice deficient in GSK3α highlight pleiotropic physiological functions in cognition and pathological activity as Tau kinase
Maurin, H., Lechat, B., Dewachter, I., Ris, L., Louis, J. V., Borghgraef, P., Devijver, H., Jaworski, T., & LEUVEN, F. V. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-27 · Cited by 39
Trafficking and Targeting of NMDA Receptors
Petralia, R. S., Wenthold, R. J., & Al‐Hallaq, R. A. (2008) · Frontiers in neuroscience · doi:10.1201/9781420044157.ch8 · Cited by 45
Anisomycin injection in area CA3 of the hippocampus impairs both short-term and long-term memories of contextual fearPreprint
Remaud, J., Ceccom, J., Carponcy, J., Dugué, L., Menchon, G., Pech, S., Halley, H., Francès, B., & Dahan, L. (2014) · Learning & Memory · doi:10.1101/lm.033969.113 · Cited by 46
Environmental enrichment improves recent but not remote memory in association with a modified brain metabolic activation profile in adult mice
Léger, M., Bouët, V., Fréret, T., Darmaillacq, A., Dacher, M., Dauphin, F., Boulouard, M., & Schumann‐Bard, P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.11.022 · Cited by 39
Mid‐life environmental enrichment increases synaptic density in CA1 in a mouse model of Aβ‐associated pathology and positively influences synaptic and cognitive health in healthy ageing
Stuart, K. E., King, A. E., Fernández-Martos, C. M., Dittmann, J., Summers, M. J., & Vickers, J. C. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24156 · Cited by 39
Environmental enrichment enhances autophagy signaling in the rat hippocampus
Takahashi, T., Shimizu, K., Shimazaki, K., Toda, H., & Nibuya, M. (2014) · Brain Research · doi:10.1016/j.brainres.2014.10.026 · Cited by 39
Genetic Demonstration of a Role for Stathmin in Adult Hippocampal Neurogenesis, Spinogenesis, and NMDA Receptor-Dependent Memory
Martel, G., Uchida, S., Hevi, C., Chévere-Torres, I., Fuentes, I., Park, Y. J., Hafeez, H., Yamagata, H., Watanabe, Y., & Shumyatsky, G. P. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4541-14.2016 · Cited by 40
Similarities and differences in spatial learning and object recognition between young male C57Bl/6J mice and Sprague-Dawley rats.
Stranahan, A. M. (2011) · Behavioral Neuroscience · doi:10.1037/a0025133 · Cited by 38
Standardization of Small Animal Imaging—Current Status and Future Prospects
Mannheim, J. G., Kara, F., Doorduin, J., Fuchs, K., Reischl, G., Liang, S., Verhoye, M., Gremse, F., Mezzanotte, L., & Huisman, M. C. (2017) · Molecular Imaging and Biology · doi:10.1007/s11307-017-1126-2 · Cited by 45
Age-dependent neuron loss is associated with impaired adult neurogenesis in forebrain neuron-specific Dicer conditional knockout mice
Cheng, S., Zhang, C., Xu, C., Wang, L., Zou, X., & Chen, G. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2014.10.029 · Cited by 39
Diversity and fluctuation of spine morphology in CA1 pyramidal neurons after transient global ischemia
Ruan, Y., Lei, Z., Fan, Y., Zou, B., & Xu, Z. C. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21816 · Cited by 39
Metabotropic glutamate receptor, mGlu5, mediates enhancements of hippocampal long-term potentiation after environmental enrichment in young and old mice
Buschler, A., & Manahan‐Vaughan, D. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.06.003 · Cited by 38
Chronic exposure of gestation rat to sevoflurane impairs offspring brain development
Wang, Y., Cheng, Y., Liu, G., Tian, X., Tu, X., & Wang, J. (2011) · Neurological Sciences · doi:10.1007/s10072-011-0762-6 · Cited by 36
Effects of maternal immune activation on adult neurogenesis in the subventricular zone–olfactory bulb pathway and olfactory discrimination
Liu, Y., Lai, W., Tsay, H.-J., Wang, T., & Yu, J. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.09.007 · Cited by 37
Hippocampal neurons with stable excitatory connectivity become part of neuronal representations
Castello-Waldow, T. P., Weston, G., Ulivi, A. F., Chenani, A., Loewenstein, Y., Chen, A., & Attardo, A. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000928 · Cited by 33
Effects of enrichment predominate over those of chronic stress on fear-related behavior in male rats
Mitra, R., & Sapolsky, R. M. (2008) · Stress · doi:10.1080/10253890802379955 · Cited by 37
Environmental enrichment and neurodegenerative diseases
Li, L., & Tang, B. L. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.05.162 · Cited by 37
Life-long environmental enrichment counteracts spatial learning, reference and working memory deficits in middle-aged rats subjected to perinatal asphyxia
Galeano, P., Blanco, E., Tornatore, T. L., Romero, J. I., Holubiec, M. I., de Fonseca, F. R., & Capani, F. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00406 · Cited by 37
Virtual enriched environments in paediatric neuropsychological rehabilitation following traumatic brain injury: Feasibility, benefits and challenges
Penn, P., Rose, F. D., & Johnson, D. A. (2009) · Developmental Neurorehabilitation · doi:10.1080/17518420902739365 · Cited by 37
RC-3095, a bombesin/gastrin-releasing peptide receptor antagonist, impairs aversive but not recognition memory in rats
Roesler, R. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.12.011 · Cited by 37
Alteration of cingulate long-term plasticity and behavioral sensitization to inflammation by environmental enrichmentPreprint
Shum, F. W. F., Wu, L., Zhao, M., Toyoda, H., Xu, H., Ren, M., Pinaud, R., Ko, S. W., Lee, Y., Kaang, B., et al. (2007) · Learning & Memory · doi:10.1101/lm.530607 · Cited by 39
Reversal of age-associated memory impairment by rosuvastatin in rats
Rech, R. L., de Lima, M. N. M., Dornelles, A., Garcia, V. A., Alcalde, L. A., Vedana, G., & Schröder, N. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.02.001 · Cited by 35
Post‐weaning environmental enrichment improves BDNF response of adult male rats
Mosaferi, B., Babri, S., Mohaddes, G., Khamnei, S., & Abbasi, M. M. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.07.008 · Cited by 35
Acute administration of toluene affects memory retention in novel object recognition test and memory function‐related gene expression in mice
Win‐Shwe, T., & Fujimaki, H. (2011) · Journal of Applied Toxicology · doi:10.1002/jat.1693 · Cited by 36
Neuregulin 1: a prime candidate for research into gene-environment interactions in schizophrenia? Insights from genetic rodent models
Karl, T. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00106 · Cited by 37
Environmental stimulation rescues maternal high fructose intake-impaired learning and memory in female offspring: Its correlation with redistribution of histone deacetylase 4
Wu, K. L. H., Wu, C., Tain, Y., Huang, L., Chao, Y., Hung, C., Wu, J., Chen, S.-R., Tsai, P.-C., & Chan, J. Y. H. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.02.004 · Cited by 38
A single exposure to an enriched environment stimulates the activation of discrete neuronal populations in the brain of the fos-tau-lacZ mouse
Ali, A. E. A., Wilson, Y. M., & Murphy, M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.05.004 · Cited by 36

Authors: Rampon, C., Tang, Y.-P., Goodhouse, J., Shimizu, E., Kyin, M., & Tsien, J. Z.
Affiliations: Princeton University (US)
Corresponding author: Tsien, Joe Z.
ORCID: Rampon, Claire
Tang, Ya-Ping
Shimizu, Eiji
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2000-03-01
Volume: 3
Issue: 3
Pages: 238-244
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/72945
OpenAlex: W1481984979
Semantic Scholar: fa40536e2cbc3bd383f248197b5f4cb17804cd65
Cited by: 755
References: 41
Citations by year: 2026: 3 · 2025: 8 · 2024: 9 · 2023: 20 · 2022: 12 · 2021: 16 · 2020: 20 · 2019: 20 · 2018: 22 · 2017: 22 · 2016: 32 · 2015: 30 · 2014: 33 · 2013: 40 · 2012: 44
FWCI: 15.59
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Foundation for the National Institutes of Health
Arnold and Mabel Beckman Foundation
Princeton University
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: NMDA receptor 1, CA1, hippocampus, memory impairment, object recognition memory, odor discrimination, contextual fear memory, environmental enrichment, synaptic plasticity, synaptic density, knockout mice, memory recovery
MeSH terms: Animals, Conditioning, Psychological, Cues, Dendrites, Electroshock, Exploratory Behavior, Fear, Female, Food Preferences, Male, Memory, Memory Disorders, Pattern Recognition, Visual, Smell, Space Perception, Synapses, Receptors, N-Methyl-D-Aspartate, Long-Term Potentiation, Pyramidal Cells, Mice, Knockout, Mice

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

Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks