Matrix metalloproteinase-9 regulates neuronal circuit development and excitability
Open accessAbstract
In early postnatal development, naturally occurring cell death, dendritic outgrowth, and synaptogenesis sculpt neuronal ensembles into functional neuronal circuits. Here, we demonstrate that deletion of the extracellular proteinase matrix metalloproteinase-9 (MMP-9) affects each of these processes, resulting in maladapted neuronal circuitry. MMP-9 deletion increases the number of CA1 pyramidal neurons but decreases dendritic length and complexity. Parallel changes in neuronal morphology are observed in primary visual cortex and persist into adulthood. Individual CA1 neurons in MMP-9(-/-) mice have enhanced input resistance and a significant increase in the frequency, but not amplitude, of miniature excitatory postsynaptic currents (mEPSCs). Additionally, deletion of MMP-9 significantly increases spontaneous neuronal activity in awake MMP-9(-/-) mice and enhances response to acute challenge by the excitotoxin kainate. Our data document a novel role for MMP-9-dependent proteolysis: the regulation of several aspects of circuit maturation to constrain excitability throughout life.
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?
RS neurons in Mmp9−/− visual cortex have elevated excitability and reduced dendritic spine density.
“However, RS neurons in Mmp9−/− visual cortex have elevated excitability and reduced dendritic spine density, as previously reported (Murase et al., 2016; Kelly et al., 2015).”
From Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9 (2017) · cites this paper as Murase et al., 2016
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
Philosophical transactions of the Royal Society of London. B
Press, H. (1886) · Cited by 10,087 · see citing works
Hynes (2002) · doi:10.1016/s0092-8674(02)00971-6 · Cited by 8,606 · see citing works
Modification of seizure activity by electrical stimulation: II. Motor seizure
Racine, R. J. (1972) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(72)90177-0 · Cited by 7,141 · see citing works
Cell death during development of the nervous system
Oppenheim, R. W. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.002321 · Cited by 3,084 · see citing works
The NEURON Simulation Environment
Hines, M. L., & Carnevale, N. T. (1997) · Neural Computation · doi:10.1162/neco.1997.9.6.1179 · Cited by 2,630 · see citing works
Molecular mechanisms of caspase regulation during apoptosis
Riedl, S. J., & Shi, Y. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1496 · Cited by 1,893 · see citing works
Ben-Ari, Y. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90299-4 · Cited by 1,753 · see citing works
Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., & Werb, Z. (1998) · Cell · doi:10.1016/s0092-8674(00)81169-1 · Cited by 1,737 · see citing works
Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons
Nagai, M., Re, D. B., Nagata, T., Chalazonitis, A., Jessell, T. M., Wichterle, H., & Przedborski, S. (2007) · Nature Neuroscience · doi:10.1038/nn1876 · Cited by 1,220 · see citing works
Linked Regularities in the Development and Evolution of Mammalian Brains
Finlay, B. L., & Darlington, R. B. (1995) · Science · doi:10.1126/science.7777856 · Cited by 1,217 · see citing works
Harris, K. M., Jensen, F. E., & Tsao, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02685.1992 · Cited by 990 · see citing works
Mitra, P. P., & Bokil, H. (2007) · doi:10.1093/acprof:oso/9780195178081.001.0001 · Cited by 819 · see citing works
Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia
Garey, L. J., Ong, W., Patel, T. S., Kanani, M., Davis, A., Mortimer, A. M., Barnes, T., & Hirsch, S. R. (1998) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.65.4.446 · Cited by 719 · see citing works
Activity-dependent regulation of dendritic growth and patterning
Wong, R. O. L., & Ghosh, A. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn941 · Cited by 635 · see citing works
Inactivity produces increases in neurotransmitter release and synapse size
Murthy, V. N., Schikorski, T., Stevens, C. F., & Zhu, Y. (2001) · Neuron · doi:10.1016/s0896-6273(01)00500-1 · Cited by 612 · see citing works
Epileptogenesis in the immature brain: emerging mechanisms
Rakhade, S. N., & Jensen, F. E. (2009) · Nature Reviews Neurology · doi:10.1038/nrneurol.2009.80 · Cited by 554 · see citing works
Adaptation to Synaptic Inactivity in Hippocampal Neurons
Thiagarajan, T. C., Lindskog, M., & Tsien, R. W. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.037 · Cited by 482 · see citing works
Bilousova, T. V., Dansie, L., Ngo, M., Aye, J., Charles, J. R., Ethell, D. W., & Ethell, I. M. (2009) · Journal of Medical Genetics · doi:10.1136/jmg.2008.061796 · Cited by 465 · see citing works
Gu, Z., Cui, J.-K., Brown, S. M., Fridman, R., Mobashery, S., Strongin, A., & Lipton, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1563-05.2005 · Cited by 412 · see citing works
Szklarczyk, A., Lapinska, J., Rylski, M., McKay, R. D. G., & Kaczmarek, L. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00920.2002 · Cited by 392 · see citing works
Laminin is associated with the "neurite outgrowth-promoting factors" found in conditioned media.
Lander, A. D., Fujii, D. K., & Reichardt, L. F. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.7.2183 · Cited by 346 · see citing works
Neuroinflammation and white matter pathology in schizophrenia: systematic review
Najjar, S., & Pearlman, D. M. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.04.041 · Cited by 317 · see citing works
Wang, X.-B., Bozdagi, O., Nikitczuk, J. S., Zhai, Z. W., Zhou, Q., & Huntley, G. W. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807248105 · Cited by 316 · see citing works
Epilepsy in autism spectrum disorders
Canitano, R. (2006) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-006-0563-2 · Cited by 308 · see citing works
Dendritic Spine Loss and Synaptic Alterations in Alzheimer’s Disease
Knobloch, M., & Mansuy, I. M. (2008) · Molecular Neurobiology · doi:10.1007/s12035-008-8018-z · Cited by 296 · see citing works
Important role of matrix metalloproteinase 9 in epileptogenesis
Wilczynski, G. M., Konopacki, F. A., Wilczek, E., Lasiecka, Z., Gorlewicz, A., Michaluk, P., Wawrzyniak, M., Malinowska, M., Okulski, P., Kolodziej, L. R., et al. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200708213 · Cited by 292 · see citing works
Synaptic circuit remodelling by matrix metalloproteinases in health and disease
Huntley, G. W. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3320 · Cited by 282 · see citing works
Fragile X syndrome: a review of associated medical problems
Kidd, S. A., Lachiewicz, A., Barbouth, D., Blitz, R. K., Delahunty, C., McBrien, D., Visootsak, J., & Berry-Kravis, E. (2014) · Pediatrics · doi:10.1542/peds.2013-4301 · Cited by 255 · see citing works
Cheng, T.-L., Wang, Z., Liao, Q., Zhu, Y., Zhou, W.-H., Xu, W., & Qiu, Z. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.01.032 · Cited by 253 · see citing works
Schizophrenia-Related Neural and Behavioral Phenotypes in Transgenic Mice Expressing TruncatedDisc1
Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S. L., Chatzi, C. A., He, S., Mackie, I., Brandon, N. J., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3299-08.2008 · Cited by 250 · see citing works
Very long-term memories may be stored in the pattern of holes in the perineuronal net
Tsien, R. Y. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310158110 · Cited by 244 · see citing works
Transsynaptic Signaling by Activity-Dependent Cleavage of Neuroligin-1
Peixoto, R. T., Kunz, P. A., Kwon, H., Mabb, A. M., Sabatini, B. L., Philpot, B. D., & Ehlers, M. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.006 · Cited by 224 · see citing works
Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology
Michaluk, P., Wawrzyniak, M., Alot, P., Szczot, M., Wyrembek, P., Mercik, K., Medvedev, N., Wilczek, E., De Roo, M., Zuschratter, W., et al. (2011) · Journal of Cell Science · doi:10.1242/jcs.090852 · Cited by 214 · see citing works
Mizoguchi, H., Nakade, J., Tachibana, M., Ibi, D., Someya, E., Koike, H., Kamei, H., Nabeshima, T., Itohara, S., Takuma, K., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3118-11.2011 · Cited by 199 · see citing works
Baj, G., Leone, E., Chao, M. V., & Tongiorgi, E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014168108 · Cited by 196 · see citing works
Koshimizu, H., Kiyosue, K., Hara, T., Hazama, S., Suzuki, S., Uegaki, K., Nagappan, G., Zaitsev, E., Hirokawa, T., Tatsu, Y., et al. (2009) · Molecular Brain · doi:10.1186/1756-6606-2-27 · Cited by 195 · see citing works
Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases
Heissig, B., Hattori, K., Friedrich, M., Rafii, S., & Werb, Z. (2003) · Current Opinion in Hematology · doi:10.1097/00062752-200303000-00007 · Cited by 186 · see citing works
Jourquin, J., Tremblay, E., Décanis, N., Charton, G., Hanessian, S., Chollet, A., Le Diguardher, T., Khrestchatisky, M., & Rivera, S. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02876.x · Cited by 178 · see citing works
Intrinsic excitability of CA1 pyramidal neurones from the rat dorsal and ventral hippocampus
Dougherty, K. A., Islam, T., & Johnston, D. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.242693 · Cited by 158 · see citing works
Sidhu, H., Dansie, L. E., Hickmott, P. W., Ethell, D. W., & Ethell, I. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1162-14.2014 · Cited by 155 · see citing works
Pfeiffer, B. E., & Huber, K. M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0054-07.2007 · Cited by 154 · see citing works
Ang, C. W., Carlson, G. C., & Coulter, D. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2354-06.2006 · Cited by 150 · see citing works
FMRP Involvement in Formation of Synapses among Cultured Hippocampal Neurons
Braun, K. A. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.1045 · Cited by 149 · see citing works
Bianchi, D., Marasco, A., Limongiello, A., Marchetti, C., Marie, H., Tirozzi, B., & Migliore, M. (2012) · Journal of Computational Neuroscience · doi:10.1007/s10827-012-0383-y · Cited by 147 · see citing works
Epilepsy in Rett syndrome, and CDKL5‐ and FOXG1‐gene–related encephalopathies
Guerrini, R., & Parrini, E. (2012) · Epilepsia · doi:10.1111/j.1528-1167.2012.03656.x · Cited by 146 · see citing works
White, A. M., Williams, P. A., Ferraro, D. J., et al. (2005) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2005.09.014 · Cited by 138 · see citing works
Synaptic plasticity mediating cocaine relapse requires matrix metalloproteinases
Smith, A. C. W., Kupchik, Y. M., Scofield, M. D., Gipson, C. D., Wiggins, A., Thomas, C. A., & Kalivas, P. W. (2014) · Nature Neuroscience · doi:10.1038/nn.3846 · Cited by 133 · see citing works
Activity-Dependent Local Translation of Matrix Metalloproteinase-9
Dziembowska, M., Miłek, J., Janusz, A., Rejmak, E., Romanowska, E., Górkiewicz, T., Tiron, A., Bramham, C. R., & Kaczmarek, L. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6028-11.2012 · Cited by 127 · see citing works
Extracellular matrix molecules, their receptors, and secreted proteases in synaptic plasticity
Włodarczyk, J., Mukhina, I. V., Kaczmarek, L., & Dityatev, A. E. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20958 · Cited by 123 · see citing works
Naturally occurring cell death in the developing dentate gyrus of the rat
Gould, E., Woolley, C. S., & McEwen, B. S. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903040306 · Cited by 120 · see citing works
The Fragile X mental retardation protein regulates matrix metalloproteinase 9 mRNA at synapses.
Janusz, A., Miłek, J., Perycz, M., Pacini, L., Bagni, C., Kaczmarek, L., & Dziembowska, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2207-13.2013 · Cited by 112 · see citing works
Gary, D. S., Milhavet, O., Camandola, S., & Mattson, M. P. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01579.x · Cited by 105 · see citing works
The metastasis-promoting S100A4 protein confers neuroprotection in brain injury
Dmytriyeva, O., Pankratova, S., Owczarek, S., Sonn, K., Soroka, V., Ridley, C. M., Marsolais, A. J., López‐Hoyos, M., Ambartsumian, N. S., Lukanidin, E. M., et al. (2012) · Nature Communications · doi:10.1038/ncomms2202 · Cited by 103 · see citing works
Ferrer, I., Tortosa, A., Blanco, R. E., Martín, F., Serrano, T., Planas, A. M., & Macaya, A. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90210-0 · Cited by 94 · see citing works
G enetically A ltered M ouse M odels: the G ood, the B ad, and the U gly
Thyagarajan, T., Totey, S. M., Danton, M. J. S., & Kulkarni, A. B. (2003) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/154411130301400302 · Cited by 92 · see citing works
Fujita, E., Dai, H., Tanabe, Y., Zhiling, Y., Yamagata, T., Miyakawa, T., Tanokura, M., Momoi, M. Y., & Momoi, T. (2010) · Cell Death and Disease · doi:10.1038/cddis.2010.23 · Cited by 90 · see citing works
Reward Learning Requires Activity of Matrix Metalloproteinase-9 in the Central Amygdala
Knapska, E., Lioudyno, V. I., Kiryk, A., Mikosz, M., Górkiewicz, T., Michaluk, P., Gawlak, M., Chaturvedi, M., Mochol, G., Balcerzyk, M., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5239-12.2013 · Cited by 87 · see citing works
Szepesi, Z., Hosy, E., Ruszczycki, B., Bijata, M., Pyskaty, M., Bikbaev, A., Heine, M., Choquet, D., Kaczmarek, L., & Wlodarczyk, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098274 · Cited by 83 · see citing works
A Specific Survival Response in Dopamine Neurons at Most Risk in Parkinson's Disease
Murase, S., & McKay, R. D. G. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2745-06.2006 · Cited by 80 · see citing works
Self-citationAsynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus
Soriano, E., Cobas, A., & Fairén, A. (1986) · Developmental Brain Research · doi:10.1016/0165-3806(86)90134-3 · Cited by 74 · see citing works
β1-Integrin and Integrin Linked Kinase Regulate Astrocytic Differentiation of Neural Stem Cells
Pan, L., North, H. A., Sahni, V., Jeong, S. J., McGuire, T. L., Berns, E. J., Stupp, S. I., & Kessler, J. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104335 · Cited by 70 · see citing works
Matrix metalloproteinase-9 (MMP-9) in human intractable epilepsy caused by focal cortical dysplasia
Konopka, A., Grajkowska, W., Ziemiańska, K., Roszkowski, M., Daszkiewicz, P., Rysz, A., Marchel, A., Koperski, Ł., Wilczynski, G. M., & Dzwonek, J. (2012) · Epilepsy Research · doi:10.1016/j.eplepsyres.2012.09.018 · Cited by 68 · see citing works
Astrocytes and extracellular matrix in extrasynaptic volume transmission
Vargová, L., & Syková, E. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0608 · Cited by 65 · see citing works
Kim, G. W., Kim, H.-J., Cho, K.-J., Kim, H.-W., Cho, Y.-J., & Lee, B. I. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.07.008 · Cited by 63 · cited 1× · see citing works
“Interestingly, seizure-induced neuronal death is mediated by the MMP-9-dependent disruption of integrin β1-PI3K/Akt signaling [66], the same survival pathway that is disrupted by MMP-9 early in neonatal natural cell death, which coincides with high MMP-9 expression levels [7].”
Spolidoro, M., Putignano, E., Munafò, C., Maffei, L., & Pizzorusso, T. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr158 · Cited by 58 · see citing works
Kaliszewska, A., Bijata, M., Kaczmarek, L., & Kossut, M. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr303 · Cited by 55 · see citing works
Genetically encoded FRET-based biosensor for imaging MMP-9 activity
Stawarski, M., Rutkowska-Włodarczyk, I., Zeug, A., Bijata, M., Madej, H., Kaczmarek, L., & Włodarczyk, J. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.11.033 · Cited by 51 · see citing works
Rohrbough, J. C., Rushton, E., Woodruff, E. A., Fergestad, T., Vigneswaran, K., & Broadie, K. S. (2007) · Genes & Development · doi:10.1101/gad.1574107 · Cited by 49 · see citing works
Extracellular proteases in epilepsy
Łukasiuk, K., Wilczynski, G. M., & Kaczmarek, L. (2011) · Epilepsy Research · doi:10.1016/j.eplepsyres.2011.08.002 · Cited by 48 · see citing works
Synaptic plasticity and signaling in rett syndrome
Sala, G. D., & Pizzorusso, T. (2013) · Developmental Neurobiology · doi:10.1002/dneu.22114 · Cited by 41 · see citing works
Murase, S., Owens, D. F., & McKay, R. D. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0202-11.2011 · Cited by 40 · see citing works
Self-citationAujla, P. K., & Huntley, G. W. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23468 · Cited by 39 · see citing works
Matrix Metalloproteinase-9 Regulates Survival of Neurons in Newborn Hippocampus
Murase, S., & McKay, R. D. G. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.297671 · Cited by 34 · see citing works
Self-citationGephyrin Regulates GABAergic and Glutamatergic Synaptic Transmission in Hippocampal Cell Cultures
Varley, Z. K., Pizzarelli, R., Antonelli, R., Stancheva, S. H., Kneussel, M., Cherubini, E., & Zacchi, P. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.234641 · Cited by 29 · see citing works
Hoehna, Y., Uckermann, O., Luksch, H., Stefovska, V. G., Marzahn, J., Theil, M., Górkiewicz, T., Gawlak, M., Wilczynski, G. M., Kaczmarek, L., et al. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.06.023 · Cited by 27 · see citing works
Stoned B mediates sorting of integral synaptic vesicle proteins
Mohrmann, R., Matthies, H. J. G., Woodruff, E. A., & Broadie, K. S. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.060 · Cited by 21 · see citing works
DP-b99 Modulates Matrix Metalloproteinase Activity and Neuronal Plasticity
Yeghiazaryan, M., Rutkowska-Włodarczyk, I., Konopka, A., Wilczynski, G. M., Melikyan, A., Korkotian, E., Kaczmarek, L., & Figiel, I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099789 · Cited by 19 · see citing works
Lack of kainic acid‐induced gamma oscillations predicts subsequent CA1 excitotoxic cell death
Jinde, S., Belforte, J. E., Yamamoto, J., Wilson, M. A., Tonegawa, S., & Nakazawa, K. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06896.x · Cited by 18 · see citing works
Asynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus
Soriano, E., Cobas, A., & Fairén, A. G. (1986) · Brain Research · doi:10.1016/s0006-8993(86)80012-9 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Matrix Metalloproteinases as New Targets in Alzheimer’s Disease: Opportunities and Challenges
Zipfel, P., Rochais, C., Baranger, K., Rivera, S., & Dallemagne, P. (2020) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.0c00352 · Cited by 94 · see citing works
Murase, S., Lantz, C. L., & Quinlan, E. M. (2017) · eLife · doi:10.7554/elife.27345 · Cited by 87 · see citing works
Self-citation
- Authors
- Murase, S., Lantz, C. L., Kim, E., Gupta, N., Higgins, R., Stopfer, M., Hoffman, D. A., & Quinlan, E. M.
- Affiliations
- National Institutes of Health (US)
- University of Maryland, College Park (US)
- Corresponding author
- Murase, Sachiko
- ORCID
- Venue
- Molecular Neurobiology
- Published
- 2015-06-21
- Volume
- 53
- Issue
- 5
- Pages
- 3477-3493
- ISSN
- 0893-7648 (ISSN-L)
- 1559-1182
- PMC
- PMC4686372
- OpenAlex
- W2196613855
- Cited by
- 35
- References
- 79
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 7 · 2019: 5 · 2018: 3 · 2017: 3 · 2016: 3 · 2015: 1
- FWCI
- 1.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Molecular Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Eye Institute (R01EY025922, R01EY016431)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- MMP-9, neural circuit development, neuronal excitability, dendritic outgrowth, synaptogenesis, CA1 pyramidal neurons, primary visual cortex, input resistance, miniature excitatory postsynaptic currents, spontaneous neuronal activity, kainate excitotoxicity, proteolysis, postnatal brain development, dendritic morphology
- MeSH terms
- Animals, Animals, Newborn, Female, Hippocampus, Kainic Acid, Male, Mice, Inbred C57BL, Nerve Net, Synaptic Transmission, Neurons, Seizures, Synapses, Biomarkers, Proto-Oncogene Proteins c-fos, Cell Death, Pyramidal Cells, Matrix Metalloproteinase 9, Dendritic Spines
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
