Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome
Open accessAbstract
Fragile X syndrome, the most frequent form of hereditary mental retardation, is due to a mutation of the fragile X mental retardation 1 ( FMR1 ) gene on the X chromosome. Like fragile X patients, FMR1 -knockout ( FMR1 -KO) mice lack the normal fragile X mental retardation protein (FMRP) and show both cognitive alterations and an immature neuronal morphology. We reared FMR1 -KO mice in a C57BL/6 background in enriched environmental conditions to examine the possibility that experience-dependent stimulation alleviates their behavioral and neuronal abnormalities. FMR1 -KO mice kept in standard cages were hyperactive, displayed an altered pattern of open field exploration, and did not show habituation. Quantitative morphological analyses revealed a reduction in basal dendrite length and branching together with more immature-appearing spines along apical dendrites of layer five pyramidal neurons in the visual cortex. Enrichment largely rescued these behavioral and neuronal abnormalities while increasing α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) glutamate receptor subunit 1 (GluR1) levels in both genotypes. Enrichment did not, however, affect FMRP levels in the WT mice. These data suggest that FMRP-independent pathways activating glutamatergic signaling are preserved in FMR1 -KO mice and that they can be elicited by environmental stimulation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Environmental enrichment (changing objects and adding a running wheel) decreased anxiety and restored dendritic length and branching, spine density and maturation in a mouse model of fragile X.
“Changing objects and adding a running wheel in the cage decreased anxiety and restored dendritic length and branching, spine density and maturation in a mouse model of fragile X 33 .”
From Progress toward treatments for synaptic defects in autism (2013) · cites this paper as [33]
In the FXS mouse model, an enriched environment reduces multiple cellular and behavioral deficits.
“an enriched environment has been reported to ameliorate several cellular and behavioral deficits in the mouse model for FXS (129, 130).”
From Fragile X syndrome: causes, diagnosis, mechanisms, and therapeutics (2012) · cites this paper as [129]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Hayashi, Y., Shi, S.-H., Esteban, J. A., Piccini, A., Poncer, J.-C., & Malinow, R. (2000) · Science · doi:10.1126/science.287.5461.2262 · Cited by 1,524 · see citing works
Altered synaptic plasticity in a mouse model of fragile X mental retardation
Huber, K. M., Gallagher, S. M., Warren, S. T., & Bear, M. F. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.122205699 · Cited by 1,349 · see citing works
PSD-95 Involvement in Maturation of Excitatory Synapses
El-Husseini, A. E.-D., Schnell, E., Chetkovich, D. M., Nicoll, R. A., & Bredt, D. S. (2000) · Science · doi:10.1126/science.290.5495.1364 · Cited by 1,303 · see citing works
Fmr1 knockout mice: A model to study fragile X mental retardation
THEDUTCHBELGIANFRAGILEXCONSOR (1994) · Cell · doi:10.1016/0092-8674(94)90569-x · Cited by 1,075 · see citing works
Abnormal dendritic spines in fragile X knockout mice: Maturation and pruning deficits
Comery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J., & Greenough, W. T. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5401 · Cited by 1,046 · see citing works
Self-citationFMR1 Protein: Conserved RNP Family Domains and Selective RNA Binding
Ashley, C. T., Wilkinson, K. D., Reines, D., & Warren, S. T. (1993) · Science · doi:10.1126/science.7692601 · Cited by 741 · see citing works
Zalfa, F., Giorgi, M., Primerano, B., Moro, A., Di Penta, A., Reis, S., Oostra, B., & Bagni, C. (2003) · Cell · doi:10.1016/s0092-8674(03)00079-5 · Cited by 676 · see citing works
Self-citationDendritic Spine Structural Anomalies in Fragile-X Mental Retardation Syndrome
Irwin, S. A. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.1038 · Cited by 626 · see citing works
A method for vibratome sectioning of Golgi–Cox stained whole rat brain
Gibb, R. L., & Kolb, B. E. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(97)00163-5 · Cited by 618 · see citing works
Effects of environmental enrichment on gene expression in the brain
Rampon, C., Jiang, C. H., Dong, H., Tang, Y., Lockhart, D. J., Schultz, P. G., Tsien, J. Z., & Hu, Y. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.23.12880 · Cited by 614 · see citing works
Abnormal Development of Dendritic Spines in<i>FMR1</i>Knock-Out Mice
Nimchinsky, E. A., Oberlander, A. M., & Svoboda, K. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05139.2001 · Cited by 560 · see citing works
Long-Term Environmental Enrichment Leads to Regional Increases in Neurotrophin Levels in Rat Brain
Ickes, B. R., Pham, T. M., Sanders, L., Albeck, D. S., Mohammed, A. H. S., & Granholm, A. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7415 · Cited by 541 · see citing works
A Decade of Molecular Studies of Fragile X Syndrome
O'Donnell, W. T., & Warren, S. T. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142909 · Cited by 481 · see citing works
Turner, A. M., & Greenough, W. T. (1985) · Brain Research · doi:10.1016/0006-8993(85)90525-6 · Cited by 459 · see citing works
Glutamate receptors regulate actin-based plasticity in dendritic spines
Fischer, M., Kaech, S., Wagner, U., Brinkhaus, H., & Matus, A. (2000) · Nature Neuroscience · doi:10.1038/78791 · Cited by 446 · see citing works
Benaroya‐Milshtein, N., Hollander, N., Apter, A., Kukulansky, T., Raz, N., Wilf, A., Yaniv, I., & Pick, C. G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03587.x · Cited by 439 · see citing works
The effects of early experience on problem-solving at maturity
Hebb, D. O. (1947) · American Psychologist · Cited by 425 · see citing works
Griebel, G., Belzung, C., Perrault, G., & Sanger, D. J. (2000) · Psychopharmacology · doi:10.1007/s002130050038 · Cited by 420 · see citing works
Tissue specific expression of FMR-1 provides evidence for a functional role in fragile X syndrome
Hinds, H. L., Ashley, C. T., Sutcliffe, J. S., Nelson, D. L., Warren, S. T., Housman, D. E., & Schalling, M. (1993) · Nature Genetics · doi:10.1038/ng0193-36 · Cited by 396 · see citing works
Antar, L. N., Afroz, R., Dictenberg, J. B., Carroll, R. C., & Bassell, G. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0099-04.2004 · Cited by 389 · see citing works
Glaser, E. M., & der Loos, H. V. (1981) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(81)90045-5 · Cited by 374 · see citing works
Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat
Greenough, W. T., Volkmar, F. R., & Juraska, J. M. (1973) · Experimental Neurology · doi:10.1016/0014-4886(73)90278-1 · Cited by 370 · see citing works
Understanding the molecular basis of fragile X syndrome
Jin, P. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.6.901 · Cited by 368 · see citing works
Synaptic regulation of protein synthesis and the fragile X protein
Greenough, W. T., Klintsova, A. Y., Irwin, S. A., Galvez, R., Bates, K. E., & Weiler, I. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141145998 · Cited by 317 · see citing works
PSD‐95 regulates synaptic transmission and plasticity in rat cerebral cortex
Béïque, J.-C., & Andrade, R. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.031369 · Cited by 313 · see citing works
Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice
Frick, K. M., & Fernandez, S. M. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00138-0 · Cited by 303 · see citing works
Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2
Passafaro, M., Nakagawa, T., Sala, C., & Sheng, M. (2003) · Nature · doi:10.1038/nature01781 · Cited by 301 · see citing works
Schrijver, N. C. A., Bahr, N. I., Weiss, I. C., & Würbel, H. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00790-6 · Cited by 294 · see citing works
Effects of environmental complexity and training on brain chemistry.
Krech, D., Rosenzweig, M. R., & Bennett, E. L. (1960) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0045402 · Cited by 293 · see citing works
Todd, P. K., Mack, K. J., & Malter, J. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2336265100 · Cited by 280 · see citing works
Li, J., Pelletier, M. R., Perez-Velazquez, J. L., & Carlen, P. L. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2001.1085 · Cited by 271 · see citing works
Irwin, S. A., Idupulapati, M., Gilbert, M. E., Harris, J. B., Chakravarti, A. B., Rogers, E. J., Crisostomo, R. A., Larsen, B. P., Mehta, A., Alcantara, C. J., et al. (2002) · American Journal of Medical Genetics · doi:10.1002/ajmg.10500 · Cited by 270 · see citing works
Self-citationThe fragile X premutation: into the phenotypic fold
Hagerman, R. J., & Hagerman, P. J. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00299-x · Cited by 259 · see citing works
Behavioral and neuroanatomical characterization of the <i>Fmr1</i> knockout mouse
Mineur, Y. S., Sluyter, F., de Wit, S., Oostra, B. A., & Crusio, W. E. (2002) · Hippocampus · doi:10.1002/hipo.10005 · Cited by 216 · see citing works
A Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment
Faherty, C. J., Kerley, D. A., & Smeyne, R. J. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00642-9 · Cited by 210 · see citing works
Hessl, D., Dyer-Friedman, J., Glaser, B., Wisbeck, J., Barajas, R. G., Taylor, A., & Reiss, A. L. (2001) · Pediatrics · doi:10.1542/peds.108.5.e88 · Cited by 201 · see citing works
Environmental enrichment: Effects on spatial memory and hippocampal CREB immunoreactivity
Williams, B. M., Luo, Y. M., Ward, C. P., Redd, K. J., Gibson, R., Kuczaj, S. A., & McCoy, J. G. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00543-1 · Cited by 191 · see citing works
Nithianantharajah, J. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.02.002 · Cited by 191 · see citing works
The metric analysis of three-dimensional dendritic tree patterns: a methodological review
Uylings, H. B. M., Ruiz‐Marcos, A., & van Pelt, J. (1986) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(86)90116-0 · Cited by 187 · see citing works
Nielsen, D. M., Derber, W. J., McClellan, D. A., & Crnic, L. S. (2002) · Brain Research · doi:10.1016/s0006-8993(01)03309-1 · Cited by 154 · see citing works
Learning-disabled Males With a Fragile X CGG Expansion in the Upper Premutation Size Range
Hagerman, R. J., Staley, L. W., O'Conner, R., Lugenbeel, K. A., Nelson, D. L., McLean, S. D., & Taylor, A. K. (1996) · PEDIATRICS · doi:10.1542/peds.97.1.122 · Cited by 124 · see citing works
Galvez, R., Gopal, A. R., & Greenough, W. T. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02363-1 · Cited by 118 · see citing works
Gabel, L. A., Won, S., Kawai, H. D., McKinney, M., Tartakoff, A. M., & Fallon, J. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2185-04.2004 · Cited by 103 · see citing works
Genetic and Environmental Influences on the Cognitive Outcomes of Children With Fragile X Syndrome
DYER-FRIEDMAN, J., GLASER, B., HESSL, D., JOHNSTON, C., HUFFMAN, L. C., TAYLOR, A., WISBECK, J., & REISS, A. L. (2002) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200203000-00002 · Cited by 100 · see citing works
Increased rates of cerebral glucose metabolism in a mouse model of fragile X mental retardation
Qin, M., Kang, J. Y., & Smith, C. B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242377399 · Cited by 93 · see citing works
Horner, C. H., & Arbuthnott, E. R. (1991) · Europe PMC (PubMed Central) · Cited by 90 · see citing works
Lee, E. H. Y., Hsu, W., Ma, Y., Lee, P. J., & Chao, C.-C. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03032.x · Cited by 90 · see citing works
Greene, J. R. T., & Totterdell, S. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970414)380:3 · Cited by 88 · see citing works
Irwin, S. A., Swain, R. A., Christmon, C. A., Chakravarti, A. B., Weiler, I. J., & Greenough, W. T. (2000) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3914 · Cited by 84 · see citing works
The AMPA Receptor Subunit GluR1 Regulates Dendritic Architecture of Motor Neurons
Inglis, F. M., Crockett, R., Korada, S., Abraham, W. C., Hollmann, M., & Kalb, R. G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-18-08042.2002 · Cited by 81 · see citing works
Mlynarik, M., Johansson, B. B., & Ježová, D. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1296.032 · Cited by 57 · see citing works
AMPA receptor properties in adult rat hippocampus following environmental enrichment
Gagné, J., Gélinas, S., Martinoli, M., Foster, T. C., Ohayon, M. M., Thompson, R. F., Baudry, M., & Massicotte, G. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00451-x · Cited by 56 · see citing works
CX-516 Cortex pharmaceuticals.
Danysz, W. (2002) · PubMed · Cited by 34 · see citing works
Zalfa, F., & Bagni, C. (2004) · Current Issues in Molecular Biology · doi:10.21775/cimb.006.073 · Cited by 32 · see citing works
Self-citationUnderstanding the biological underpinnings of fragile X syndrome
Chiurazzi, P., Neri, G., & Oostra, B. A. (2003) · Current Opinion in Pediatrics · doi:10.1097/00008480-200312000-00003 · Cited by 29 · see citing works
Self-citationPlasticity of the Aging Cerebral Cortex
Diamond, M. C., & Connor, J. R. (1982) · Experimental brain research. Supplementum · doi:10.1007/978-3-642-68507-1_6 · Cited by 19 · see citing works
Ghribi, O., Lapierre, L., Girard, M., Ohayon, M. M., Nalbantoglu, J. N., & Massicotte, G. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:3 · Cited by 9 · see citing works
Miller (1999) · doi:10.1002/(sici)1096-8628(19990402)83:4
Irwin (2001) · doi:10.1002/1096-8628(20010115)98:2
Flagged first, then by citations
Research works printed but not linked: 6
- Comery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J. & Greenough, W. T. (1997) Proc. Natl. Acad. Sci. USA 94, 5401-5404.
- Greenough, W. T., Klintsova, A. Y., Irwin, S. A., Galvez, R., Bates, K. E. & Weiler, I. J. (2001) Proc. Natl. Acad. Sci. USA 98, 7101-7106.
- Todd, P. K., Mack, K. J. & Malter, J. S. (2003) Proc. Natl. Acad. Sci. USA 100, 14374-81437.
- Huber, K. M., Gallagher, S. M., Warren, S. T. & Bear, M. F. (2002) Proc. Natl. Acad. Sci. USA 99, 7746-7750.
- Rampon, C., Jiang, C. H., Dong, H., Tang, Y. P., Lockhart, D. J., Schultz, P. G., Tsien, J. Z. & Hu, Y. (2000) Proc. Natl. Acad. Sci. USA 97, 12880-12884.
- Qin, M., Kang, J. & Smith, C. B. (2002) Proc. Natl. Acad. Sci. USA 99, 15758-15763.
Cited by
Sorted by citations
Enriched environments, experience-dependent plasticity and disorders of the nervous system
Nithianantharajah, J., & Hannan, A. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1970 · Cited by 1,771 · see citing works
Behavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462 · see citing works
Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder
Dawson, G. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000370 · Cited by 1,138 · see citing works
Fragile X syndrome: causes, diagnosis, mechanisms, and therapeutics
Bagni, C., Tassone, F., Neri, G., & Hagerman, R. (2012) · Journal of Clinical Investigation · doi:10.1172/jci63141 · Cited by 321 · see citing works
Self-citationGenes, circuits, and precision therapies for autism and related neurodevelopmental disorders
Sahin, M., & Sur, M. (2015) · Science · doi:10.1126/science.aab3897 · Cited by 295 · see citing works
Critical period plasticity is disrupted in the barrel cortex of FMR1 knockout mice
Harlow, E. G., Till, S. M., Russell, T. A., Wijetunge, L. S., Kind, P., & Contractor, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.024 · Cited by 252 · see citing works
Henderson, C., Wijetunge, L., Kinoshita, M. N., Shumway, M., Hammond, R. S., Postma, F. R., Brynczka, C., Rush, R., Thomas, A., Paylor, R., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004218 · Cited by 249 · see citing works
Modeling fragile X syndrome in the <i>Fmr1</i> knockout mouse
Kazdoba, T. M., Leach, P. T., Silverman, J. L., & Crawley, J. N. (2014) · Intractable & Rare Diseases Research · doi:10.5582/irdr.2014.01024 · Cited by 241 · see citing works
Progress toward treatments for synaptic defects in autism
Delorme, R., Ey, E., Toro, R., Leboyer, M., Gillberg, C., & Bourgeron, T. (2013) · Nature Medicine · doi:10.1038/nm.3193 · Cited by 218 · see citing works
Deidda, G., Bozarth, I. F., & Cancedda, L. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00119 · Cited by 192 · see citing works
Meredith, R. M., Holmgren, C. D., Weidum, M., Burnashev, N., & Mansvelder, H. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.028 · Cited by 190 · see citing works
Kondo, M., Gray, L. J., Pelka, G. J., Christodoulou, J., Tam, P. P. L., & Hannan, A. J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06305.x · Cited by 190 · see citing works
Genetic-background modulation of core and variable autistic-like symptoms in Fmr1 knock-out mice
Pietropaolo, S., Guilleminot, A., Martin, B., D'Amato, F. R., & Crusio, W. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017073 · Cited by 178 · see citing works
Longitudinal patterns of repetitive behavior in toddlers with autism
Wolff, J. J., Botteron, K. N., Dager, S. R., Elison, J. T., Estes, A. M., Gu, H., Hazlett, H. C., Pandey, J., Paterson, S. J., Schultz, R. T., et al. (2014) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12207 · Cited by 170 · see citing works
Larson, J., Jessen, R. E., Kim, D., Fine, A.-K. S., & du Hoffmann, J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2638-05.2005 · Cited by 135 · see citing works
Kas, M. J., Glennon, J. C., Buitelaar, J., Ey, E., Biemans, B., Crawley, J., Ring, R. H., Lajonchere, C., Esclassan, F., Talpos, J., et al. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3268-5 · Cited by 132 · see citing works
Lindemann, L., Jaeschke, G., Michalon, A., Vieira, E., Honer, M., Spooren, W., Porter, R., Hartung, T., Kolczewski, S., Büttelmann, B., et al. (2011) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.111.185660 · Cited by 118 · see citing works
Genetic manipulation of STEP reverses behavioral abnormalities in a fragile X syndrome mouse model
Goebel‐Goody, S. M., Wilson‐Wallis, E. D., Royston, S., Tagliatela, S. M., Naegele, J. R., & Lombroso, P. J. (2012) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2012.00781.x · Cited by 108 · see citing works
Dissociation of social and nonsocial anxiety in a mouse model of fragile X syndrome.
Liu, Z.-H., & Smith, C. B. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.02.066 · Cited by 112 · see citing works
Champagne, F. A. (2010) · Perspectives on Psychological Science · doi:10.1177/1745691610383494 · Cited by 110 · see citing works
Torrioli, M. G., Vernacotola, S., Peruzzi, L., Tabolacci, E., Mila, M., Militerni, R., Musumeci, S., Ramos, F. J., Frontera, M., Sorge, G., et al. (2008) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.32268 · Cited by 100 · see citing works
Environmental enrichment is associated with rapid volumetric brain changes in adult mice
Scholz, J., Allemang-Grand, R., Dazai, J., & Lerch, J. P. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.01.027 · Cited by 90 · see citing works
Physical activity and brain development
Gomes da Silva, S., & Arida, R. M. (2015) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2015.1077115 · Cited by 89 · see citing works
Madinier, A., Quattromani, M. J., Sjölund, C., Ruscher, K., & Wieloch, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093121 · Cited by 82 · see citing works
Early life stress inhibits expression of a novel innate immune pathway in the developing hippocampus
Wei, L., Simen, A., Mane, S., & Kaffman, A. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.239 · Cited by 71 · see citing works
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
Reynolds, S., Lane, S. J., & Richards, L. (2010) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-010-9053-4 · Cited by 54 · see citing works
Indah Winarni, T., Chonchaiya, W., Adams, E., Au, J., Mu, Y., Rivera, S. M., Nguyen, D. V., & Hagerman, R. J. (2012) · Autism Research and Treatment · doi:10.1155/2012/104317 · Cited by 52 · see citing works
Striatal atrophy and dendritic alterations in a knock-in mouse model of Huntington's disease
Lerner, R. P., Trejo Martinez, L. D. C. G., Zhu, C., Chesselet, M.-F., & Hickey, M. A. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2012.01.012 · Cited by 51 · see citing works
De Rubeis, S., Fernández, E., Buzzi, A., Di Marino, D., & Bagni, C. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-7091-0932-8_23 · Cited by 48 · see citing works
Self-citationWang, Y., Sakano, H., Beebe, K., Brown, M. R., de Laat, R., Bothwell, M., Kulesza, R. J., & Rubel, E. W. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23520 · Cited by 40 · see citing works
- Authors
- Restivo, L., Ferrari, F., Passino, E., Sgobio, C., Bock, J., Oostra, B. A., Bagni, C., & Ammassari-Teule, M.
- Affiliations
- Erasmus MC (NL)
- Laboratory of Psychobiology, Consiglio Nazionale delle Ricerche Institute of Neuroscience, 00179 Rome, Italy; Department of Experimental Neurology, Fondazione Santa Lucia, Istituto Ricovero e Cura a Carattere Scientifico, 00179 Rome, Italy; Institute of Biology, Department of Zoology and Developmental Neurobiology, Otto-von-Guericke University, 39118 Magdeburg, Germany; Department of Clinical Genetics, Erasmus Medical Center, 3015 GE Rotterdam, The Netherlands; and Department of Biology, University...
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2005-08-02
- Volume
- 102
- Issue
- 32
- Pages
- 11557-11562
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1183589
- OpenAlex
- W2060412896
- Cited by
- 299
- References
- 59
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 8 · 2023: 11 · 2022: 13 · 2021: 5 · 2020: 8 · 2019: 17 · 2018: 15 · 2017: 19 · 2016: 21 · 2015: 16 · 2014: 26 · 2013: 19 · 2012: 19
- FWCI
- 7.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- Lirias (submittedVersion, other-oa)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Funders
- Consiglio Nazionale delle Ricerche
- National Institutes of Health
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (5R01 HD 38038, R01HD038038)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Down syndrome and intellectual disability research
- Keywords
- fragile X syndrome, Fmr1 knockout mice, FMRP, environmental enrichment, behavioral recovery, dendritic morphology, dendritic spines, pyramidal neurons, visual cortex, hyperactivity, habituation, GluR1, AMPA receptors, glutamatergic signaling, experience-dependent plasticity, intellectual disability
- MeSH terms
- Animals, Behavioral Symptoms, Dendrites, Environment, Controlled, Exploratory Behavior, Fragile X Syndrome, Habituation, Psychophysiologic, Mice, Inbred C57BL, Visual Cortex, Blotting, Western, Receptors, AMPA, Mice, Knockout, Mice, Fragile X Messenger Ribonucleoprotein 1
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
