Cognitive disruption and altered hippocampus synaptic function in Reelin haploinsufficient mice
Abstract
The heterozygote reeler mouse (HRM) shows many neuroanatomical and biochemical features that are also present in some human cognitive disorders, such as schizophrenia. In the present study, hippocampal dependent plasticity and cognitive function of the HRM were characterized in detail in an attempt to reveal phenotypic functional differences that result from Reelin haploinsufficiency. The HRM and wild type mice show similar levels of overall activity, coordination, thermal nociception, startle responses, and anxiety-like behavior. In addition, both genotypes show similar shock threshold, identical cued freezing behavior and comparable spatial learning in Morris water maze tasks. However, a significant reduction in contextual fear conditioned learning was observed in the HRM. Electrophysiological studies in hippocampal CA1 synapses revealed a plethora of differences between genotypes. The HRM exhibits reduced field excitatory postsynaptic potentials in responses to similar synaptic inputs, lowered paired pulse facilitation ratio and impaired long-term depression and tetanus-induced long-term potentiation (LTP). Also, deficits were detected in LTP elicited by theta burst stimulation or by a whole cell pairing protocol. These physiologic differences could not be accounted for by changes in the overall amount of glutamate receptor subunits. In addition, it was determined that network-driven excitatory and inhibitory activities recorded in CA1 pyramidal neurons showed that the HRM had comparable amplitude and frequency of spontaneous excitatory postsynaptic currents, but a marked reduction in spontaneous inhibitory postsynaptic currents. Thus, the HRM exhibits a specific hippocampal-dependent learning deficit accompanied with a pronounced impairment of hippocampal plasticity and functional inhibitory innervation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
In the adult brain, Reelin signaling is important for memory and synaptic plasticity.
“In the adult brain, Reelin signaling is important for memory and synaptic plasticity, as deletion of either Reelin (Reln) or its receptors, Vldlr and Apoer2, impairs hippocampal synaptic transmission.”
From Deletion of neuronal <i>Idol</i> ameliorates Alzheimer's disease–related pathologies via APOE receptors (2025) · cites this paper as [78]
HRM mice have reduced short-term contextual fear learning and deficient long-term association of both forms of fear memory.
“Reelin's role in fear memory is further supported by the observations that HRM mice have reduced short-term contextual fear learning (32) and deficient longterm association of both forms of fear memory (33).”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [32]
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729 · see citing works
A protein related to extracellular matrix proteins deleted in the mouse mutant reeler
D'Arcangelo, G., G. Miao, G., Chen, S.-C., Scares, H. D., Morgan, J. I., & Curran, T. (1995) · Nature · doi:10.1038/374719a0 · Cited by 1,748 · see citing works
Decreased Dendritic Spine Density on Prefrontal Cortical Pyramidal Neurons in Schizophrenia
Glantz, L. A., & Lewis, D. A. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.1.65 · Cited by 1,636 · see citing works
Synaptic plasticity: LTP and LTD
Bear, M. F., & Malenka, R. C. (1994) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(94)90101-5 · Cited by 1,355 · see citing works
Rapid Spine Delivery and Redistribution of AMPA Receptors After Synaptic NMDA Receptor Activation
Shi, S.-H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K., & Malinow, R. (1999) · Science · doi:10.1126/science.284.5421.1811 · Cited by 1,276 · see citing works
Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., & Herz, J. (1999) · Cell · doi:10.1016/s0092-8674(00)80782-5 · Cited by 1,261 · see citing works
Prestimulus Effects on Human Startle Reflex in Normals and Schizophrenics
BRAFF, D. L., Stone, C., Callaway, E., Geyer, M. A., Glick, I. D., & Bali, L. (1978) · Psychophysiology · doi:10.1111/j.1469-8986.1978.tb01390.x · Cited by 1,171 · see citing works
Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity
Lee, H.-K., Barbarosie, M., Kameyama, K., Bear, M. F., & Huganir, R. L. (2000) · Nature · doi:10.1038/35016089 · Cited by 1,116 · see citing works
Defined types of cortical interneurone structure space and spike timing in the hippocampus
Somogyi, P., & Klausberger, T. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.078915 · Cited by 927 · see citing works
The reduced neuropil hypothesis: a circuit based model of schizophrenia
Selemon, L. D., & Goldman-Rakic, P. S. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00281-9 · Cited by 909 · see citing works
Ogawa, M., Miyata, T., Nakajimat, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., & Mikoshibat, K. (1995) · Neuron · doi:10.1016/0896-6273(95)90329-1 · Cited by 889 · cited 1× · see citing works
“Reelin is a large extracellular matrix glycoprotein that is secreted by cortical Cajal–Retzius cells located in the marginal zone during embryonic development and serves as a positioning cue for the ventricular migrating neurons (Ogawa et al., 1995; SchiVmann, Bernier, & GoYnet, 1997).”
BackgroundAutosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations
Hong, S. E., Shugart, Y. Y., Huang, D. T.-C., Shahwan, S. A., Grant, P. E., Hourihane, J. O., Martin, N. D. T., & Walsh, C. A. (2000) · Nature Genetics · doi:10.1038/79246 · Cited by 878 · see citing works
Contrasting properties of two forms of long-term potentiation in the hippocampus
Nicoll, R., & Malenka, R. (1995) · Nature · doi:10.1038/377115a0 · Cited by 854 · see citing works
Reelin Is a Ligand for Lipoprotein Receptors
D'Arcangelo, G., Homayouni, R., Keshvara, L., Rice, D. S., Sheldon, M., & Curran, T. (1999) · Neuron · doi:10.1016/s0896-6273(00)80860-0 · Cited by 808 · see citing works
Lee, H.-K., Takamiya, K., Han, J.-S., Man, H., Kim, C.-H., Rumbaugh, G., Yu, S., Ding, L., He, C., Petralia, R. S., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00122-3 · Cited by 802 · see citing works
A decrease of reelin expression as a putative vulnerability factor in schizophrenia
Impagnatiello, F., Guidotti, A. R., Pesold, C., Dwivedi, Y., Caruncho, H. J., Pisu, M. G., Uzunov, D. P., Smalheiser, N. R., Davis, J. M., Pandey, G. N., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15718 · Cited by 753 · see citing works
Tissir, F., & Goffinet, A. M. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1113 · Cited by 748 · see citing works
Neuronal position in the developing brain is regulated by mouse disabled-1
Howell, B. W., Hawkes, R., Soriano, P., & Cooper, J. A. (1997) · Nature · doi:10.1038/39607 · Cited by 692 · see citing works
Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning
Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Förster, E., Sweatt, J. D., & Herz, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205147200 · Cited by 623 · see citing works
Self-citationReelin Binds α3β1 Integrin and Inhibits Neuronal Migration
Dulabon, L., Olson, E. C., Taglienti, M. G., Eisenhuth, S., McGrath, B., Walsh, C. A., Kreidberg, J. A., & Anton, E. S. (2000) · Neuron · doi:10.1016/s0896-6273(00)00007-6 · Cited by 577 · see citing works
Reelin promoter hypermethylation in schizophrenia
Grayson, D. R., Jia, X., Chen, Y., Sharma, R. P., Mitchell, C. P., Guidotti, A., & Costa, E. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503736102 · Cited by 553 · see citing works
Presynaptic Specificity of Endocannabinoid Signaling in the Hippocampus
Wilson, R. I., Kunos, G., & Nicoll, R. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00372-5 · Cited by 543 · see citing works
Davis, S., Butcher, S., & Morris, R. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-01-00021.1992 · Cited by 539 · see citing works
Beffert, U., Weeber, E. J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J. D., Li, W.-P., Adelmann, G., Frotscher, M., Hammer, R. E., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.07.007 · Cited by 497 · see citing works
Self-citationPesold, C., Impagnatiello, F., Pisu, M. G., Uzunov, D. P., Costa, E., Guidotti, A., & Caruncho, H. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3221 · Cited by 391 · see citing works
Abdolmaleky, H. M., Cheng, K., Russo, A. L., Smith, C. L., Faraone, S. V., Wilcox, M., Shafa, R., Glatt, S. J., Nguyen, G. H., Ponte, J. F., et al. (2005) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30140 · Cited by 390 · see citing works
Avital, A., Goshen, I., Kamsler, A., Segal, M., Iverfeldt, K., Richter‐Levin, G., & Yirmiya, R. (2003) · Hippocampus · doi:10.1002/hipo.10135 · Cited by 375 · see citing works
Fatemi, S. H., Stary, J. M., Earle, J. A., Araghi‐Niknam, M., & Eagan, E. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2004.02.017 · Cited by 300 · see citing works
Reelin signaling is impaired in autism
Fatemi, S. H., Snow, A. V., Stary, J. M., Araghi-Niknam, M., Reutiman, T. J., Lee, S., Brooks, A. I., & Pearce, D. A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.018 · Cited by 280 · see citing works
Lu, Y. M., Mansuy, I. M., Kandel, E. R., & Roder, J. (2000) · Neuron · doi:10.1016/s0896-6273(00)81150-2 · Cited by 280 · see citing works
GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon
Guidotti, A., Auta, J., Davis, J. M., Dong, E., Grayson, D. R., Veldic, M., Zhang, X., & Costa, E. (2005) · Psychopharmacology · doi:10.1007/s00213-005-2212-8 · Cited by 262 · see citing works
Tremolizzo, L., Doueiri, M.-S., Dong, E., Grayson, D. R., Davis, J. M., Pinna, G., Tueting, P. A., Rodriguez‐Menendez, V., Costa, E., & Guidotti, A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.11.046 · Cited by 257 · see citing works
Förster, E., Tielsch, A., Saum, B., Weiss, K. H., Johanssen, C., Graus-Porta, D., Müller, U., & Frotscher, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202035899 · Cited by 254 · see citing works
Reelin mRNA Expression During Mouse Brain Development
Schiffmann, S. N., Bernier, B., & Goffinet, A. M. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01456.x · Cited by 227 · see citing works
Liu, W., Pesold, C., Rodríguez, M. Á., Carboni, G., Auta, J., Lacor, P. N., Larson, J., Condie, B. G., Guidotti, A., & Costa, E. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051614698 · Cited by 226 · see citing works
The phenotypic characteristics of heterozygous reeler mouse
Tueting, P. A., Costa, E., Dwivedi, Y. K., Guidotti, A., Impagnatiello, F., Manev, R. M., & Pesold, C. (1999) · Neuroreport · doi:10.1097/00001756-199904260-00032 · Cited by 221 · see citing works
Interaction of reelin signaling and Lis1 in brain development
Assadi, A. H., Zhang, G., Beffert, U., McNeil, R. S., Renfro, A., Niu, S., Quattrocchi, C. C., Antalffy, B. A., Sheldon, M., Armstrong, D. D., et al. (2003) · Nature Genetics · doi:10.1038/ng1257 · Cited by 219 · see citing works
Analysis of the RELN gene as a genetic risk factor for autism
Skaar, D. A., Shao, Y., Haines, J. L., Stenger, J. E., Jaworski, J. M., Martin, E. R., DeLong, G. R., Moore, J. H., McCauley, J. L., Sutcliffe, J. S., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001614 · Cited by 197 · see citing works
Costa, E., Davis, J. M., Grayson, D. R., Guidotti, A., Pappas, G. D., & Pesold, C. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2001.0436 · Cited by 197 · see citing works
Rodríguez, M. Á., Pesold, C., Liu, W. S., Kriho, V., Guidotti, A., Pappas, G. D., & Costa, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050589797 · Cited by 178 · see citing works
Evidence for altered trisynaptic circuitry in schizophrenic hippocampus
Benes, F. M. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00136-5 · Cited by 170 · see citing works
Fatemi, S. H. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000129 · Cited by 151 · see citing works
Altered levels of Reelin and its isoforms in schizophrenia and mood disorders
Fatemi, S. H., Kroll, J., & Stary, J. M. (2001) · Neuroreport · doi:10.1097/00001756-200110290-00014 · Cited by 149 · see citing works
Sinagra, M., Verrier, D., Frankova, D., Korwek, K. M., Blahos, J., Weeber, E. J., Manzoni, O. J., & Chavis, P. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1757-05.2005 · Cited by 128 · see citing works
Self-citationBehavioral Phenotype of the Reeler Mutant Mouse: Effects of Reln Gene Dosage and Social Isolation.
Salinger, W. L., Ladrow, P. R., & Wheeler, C. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.6.1257 · Cited by 120 · see citing works
A reelin–integrin receptor interaction regulates Arc mRNA translation in synaptoneurosomes
Dong, E., Caruncho, H. J., Liu, W., Smalheiser, N. R., Grayson, D. R., Costa, E., & Guidotti, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1031602100 · Cited by 105 · see citing works
The heterozygote reeler mouse as a model for the development of a new generation of antipsychotics
Costa, E. (2002) · Current Opinion in Pharmacology · doi:10.1016/s1471-4892(01)00121-7 · Cited by 100 · see citing works
Segregation and Coactivation of Developing Neocortical Layer 1 Neurons
Soda, T., Nakashima, R., Watanabe, D., Nakajima, K., Pastan, I. H., & Nakanishi, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-15-06272.2003 · Cited by 91 · see citing works
Pappas, G. D., Kriho, V., & Pesold, C. (2002) · Journal of Neurocytology · doi:10.1023/a:1015017710332 · Cited by 89 · see citing works
Mienville, J., & Pesold, C. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01636.1999 · Cited by 87 · see citing works
GABA-ergic neurons and the neurobiology of schizophrenia and other psychoses
Keverne, E. B. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00025-8 · Cited by 86 · see citing works
Reelin, Integrin and Dab1 Interactions during Embryonic Cerebral Cortical Development
Schmid, R. S., Jo, R., Shelton, S., Kreidberg, J. A., & Anton, E. S. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi041 · Cited by 86 · see citing works
The role of Reelin in pathology of autism
Fatemi, S. H. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001248 · Cited by 75 · see citing works
Olfactory discrimination learning deficit in heterozygous reeler mice
Larson, J., Hoffman, J. S., Guidotti, A., & Costa, E. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02353-9 · Cited by 69 · see citing works
Kobayashi, K., Noda, Y., Matsushita, N., Nishii, K., Sawada, H., Nagatsu, T., Nakahara, D., Fukabori, R., Yasoshima, Y., Yamamoto, T., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02418.2000 · Cited by 68 · see citing works
Ballmaier, M., Zoli, M., Leo, G., Agnati, L. F., & Spano, P. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01952.x · Cited by 63 · see citing works
Marder, C. P., & Buonomano, D. V. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00112.2003 · Cited by 55 · see citing works
Rosoklija, G., Toomayan, G., Ellis, S. P., Keilp, J., Mann, J. J., Latov, N., Hays, A. P., & Dwork, A. J. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.4.349 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The dual role of the extracellular matrix in synaptic plasticity and homeostasis
Dityatev, A., Schachner, M., & Sonderegger, P. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2898 · Cited by 559 · see citing works
Reelin, lipoprotein receptors and synaptic plasticity
Herz, J., & Chen, Y. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2009 · Cited by 524 · see citing works
Extracellular Matrix: Functions in the Nervous System
Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506 · see citing works
The involvement of Reelin in neurodevelopmental disorders
Folsom, T. D., & Fatemi, S. H. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.08.015 · Cited by 275 · see citing works
Reelin and neuropsychiatric disorders
Ishii, K., Kubo, K.-I., & Nakajima, K. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00229 · Cited by 185 · see citing works
LRP8-Reelin-regulated neuronal enhancer signature underlying learning and memory formation
Telese, F., Ma, Q., Perez, P. M., Notani, D., Oh, S., Li, W., Comoletti, D., Ohgi, K. A., Taylor, H., & Rosenfeld, M. G. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.033 · Cited by 166 · see citing works
New insights into Reelin-mediated signaling pathways
Lee, G. H., & D’Arcangelo, G. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00122 · Cited by 144 · see citing works
Towards understanding the schizophrenia code: an expanded convergent functional genomics approach
Le‐Niculescu, H., Balaraman, Y., Patel, S., Tan, J., Sidhu, K., Jerome, R. E., Edenberg, H. J., Kuczenski, R., Geyer, M. A., Nurnberger, J. I., et al. (2007) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30481 · Cited by 137 · see citing works
Iafrati, J., Orejarena, M. J., Lassalle, O., Bouamrane, L., & Chavis, P. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.66 · Cited by 132 · see citing works
The extracellular matrix and synapses
Dityatev, A., & Schachner, M. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0217-1 · Cited by 128 · see citing works
Reelin in the years: controlling neuronal migration and maturation in the mammalian brain
D'Arcangelo, G. (2014) · Advances in Neuroscience · doi:10.1155/2014/597395 · Cited by 120 · see citing works
Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses
Wasser, C. R., & Herz, J. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.766782 · Cited by 111 · see citing works
“Reelin’s role in fear memory is further supported by the observations that HRM mice have reduced short-term contextual fear learning (32) and deficient longterm association of both forms of fear memory (33).”
BackgroundReelin protects against amyloid β toxicity in vivo
Lane-Donovan, C., Philips, G. T., Wasser, C. R., Durakoglugil, M. S., Masiulis, I., Upadhaya, A., Pohlkamp, T., Coskun, C., Kotti, T., Steller, L., et al. (2015) · Science Signaling · doi:10.1126/scisignal.aaa6674 · Cited by 96 · see citing works
Age-related accumulation of Reelin in amyloid-like deposits
Knuesel, I., Nyffeler, M., Mormède, C., Muhia, M., Meyer, U., Pietropaolo, S., Yee, B. K., Pryce, C. R., LaFerla, F. M., Marighetto, A., et al. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.08.011 · Cited by 94 · see citing works
Reelin-mediated signaling in neuropsychiatric and neurodegenerative diseases
Knuesel, I. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.002 · Cited by 89 · see citing works
ApoE isoform-dependent changes in hippocampal synaptic function
Korwek, K. M., Trotter, J. H., LaDu, M. J., Sullivan, P. M., & Weeber, E. J. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-21 · Cited by 89 · see citing works
Self-citationRole for Reelin in neurotransmitter release
Hellwig, S., Hack, I., Kowalski, J., Brunne, B., Jarowyj, J., Unger, A., Bock, H. H., Junghans, D., & Frotscher, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3984-10.2011 · Cited by 74 · see citing works
Fenton, E. Y., Fournier, N. M., Lussier, A. L., Romay-Tallon, R., Caruncho, H. J., & Kalynchuk, L. E. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.02.001 · Cited by 69 · see citing works
Region-specific alteration of GABAergic markers in the brain of heterozygous reeler mice
Nullmeier, S., Panther, P., Dobrowolny, H., Frotscher, M., Zhao, S., Schwegler, H., & Wolf, R. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07563.x · Cited by 43 · see citing works
Meta-analyses of RELN variants in neuropsychiatric disorders
Chen, N., Bao, Y., Xue, Y., Sun, Y., Hu, D., Meng, S., Lu, L., & Shi, J. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.05.028 · Cited by 44 · see citing works
Reelin proteolysis affects signaling related to normal synapse function and neurodegeneration
Lussier, A. L., Weeber, E. J., & Rebeck, G. W. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00075 · Cited by 31 · see citing works
Self-citationThe Reelin (RELN) gene is associated with executive function in healthy individuals.
Baune, B. T., Konrad, C., Suslow, T., Domschke, K., Birosova, E., Sehlmeyer, C., & Beste, C. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.08.002 · Cited by 25 · see citing works
Karahan, H., Hartigan, K., Al‐Amin, M. M., John, S. K., McCord, B., Wijeratne, H. R. S., Acri, D. J., Smith, D. C., Dabin, L. C., Cordero, H. M. R., et al. (2025) · Alzheimer's & Dementia · doi:10.1002/alz.70949 · Cited by 2 · see citing works
“54,78 Moreover, Reelin signaling has been demonstrated to mitigate A β -mediated synaptic impairment and tau phosphorylation.”
- Authors
- QIU, S., KORWEK, K., PRATTDAVIS, A., PETERS, M., BERGMAN, M., & WEEBER, E.
- Affiliations
- Vanderbilt University Medical Center (US)
- Corresponding author
- WEEBER, E
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2006-05
- Volume
- 85
- Issue
- 3
- Pages
- 228-242
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W2069581520
- Cited by
- 202
- References
- 59
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 7 · 2022: 11 · 2021: 10 · 2020: 10 · 2019: 5 · 2018: 7 · 2017: 8 · 2016: 14 · 2015: 16 · 2014: 11 · 2013: 12 · 2012: 8
- FWCI
- 4.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Federation for Aging Research
- National Institute on Aging
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- hippocampus, synaptic plasticity, long-term potentiation, long-term depression, contextual fear conditioning, CA1 pyramidal neurons, inhibitory postsynaptic currents, excitatory postsynaptic potentials, paired-pulse facilitation, glutamate receptor subunits, schizophrenia, cognitive impairment
- MeSH terms
- Reelin Protein, Animals, Cognition Disorders, Conditioning, Psychological, Fear, Female, Genotype, Haploidy, Heterozygote, Hippocampus, Male, Nerve Tissue Proteins, Neural Inhibition, Serine Endopeptidases, Synapses, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Maze Learning, 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
