{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,12]],"date-time":"2025-11-12T13:40:24Z","timestamp":1762954824253},"reference-count":59,"publisher":"The Company of Biologists","issue":"8","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2009,4,15]]},"abstract":"<jats:p>Spine morphogenesis mainly occurs during development as a morphological shift from filopodia-like thin protrusions to bulbous ones. We have previously reported that synaptic clustering of the actin-binding protein drebrin in dendritic filopodia governs spine morphogenesis and synaptic PSD-95 clustering. Here, we report the activity-dependent cellular mechanisms for spine morphogenesis, in which the activity of AMPA receptors (AMPARs) regulates drebrin clustering in spines by promoting drebrin stabilization. In cultured developing hippocampal neurons, pharmacological blockade of AMPARs, but not of other glutamate receptors, suppressed postsynaptic drebrin clustering without affecting presynaptic clustering of synapsin I (synapsin-1). Conversely, the enhancement of the action of AMPARs promoted drebrin clustering in spines. When we explored drebrin dynamics by photobleaching individual spines, we found that AMPAR activity increased the fraction of stable drebrin without affecting the time constant of drebrin turnover. An increase in the fraction of stable drebrin corresponded with increased drebrin clustering. AMPAR blockade also suppressed normal morphological maturation of spines and synaptic PSD-95 clustering in spines. Together, these data suggest that AMPAR-mediated stabilization of drebrin in spines is an activity-dependent cellular mechanism for spine morphogenesis.<\/jats:p>","DOI":"10.1242\/jcs.043729","type":"journal-article","created":{"date-parts":[[2009,4,1]],"date-time":"2009-04-01T17:43:09Z","timestamp":1238607789000},"page":"1211-1219","source":"Crossref","is-referenced-by-count":49,"title":["Activity of the AMPA receptor regulates drebrin stabilization in dendritic spine morphogenesis"],"prefix":"10.1242","volume":"122","author":[{"given":"Hideto","family":"Takahashi","sequence":"first","affiliation":[{"name":"Department of Neurobiology and Behavior, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan"},{"name":"ERCGSM, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hiroyuki","family":"Yamazaki","sequence":"additional","affiliation":[{"name":"Department of Neurobiology and Behavior, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kenji","family":"Hanamura","sequence":"additional","affiliation":[{"name":"Department of Neurobiology and Behavior, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuko","family":"Sekino","sequence":"additional","affiliation":[{"name":"Department of Neurobiology and Behavior, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan"},{"name":"CREST, JST, Kawaguchi, Saitama, 332-0012, Japan"},{"name":"Division of Neuronal Network, Department of Basic Medical Sciences, Institute of Medical Science, University of Tokyo, Tokyo, 1108-8639, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tomoaki","family":"Shirao","sequence":"additional","affiliation":[{"name":"Department of Neurobiology and Behavior, Gunma University Graduate School of Medicine, Maebashi, Gunma, 371-8511, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","reference":[{"key":"2021042521022693200_REF1","doi-asserted-by":"crossref","unstructured":"Allison, D. W., Gelfand, V. I., Spector, I. and Craig, A. M. (1998). Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J. Neurosci.18, 2423-2436.","DOI":"10.1523\/JNEUROSCI.18-07-02423.1998"},{"key":"2021042521022693200_REF2","doi-asserted-by":"crossref","unstructured":"Asada, H., Uyemura, K. and Shirao, T. (1994). Actin-binding protein, drebrin, accumulates in submembranous regions in parallel with neuronal differentiation. J. Neurosci. Res.38, 149-159.","DOI":"10.1002\/jnr.490380205"},{"key":"2021042521022693200_REF3","doi-asserted-by":"crossref","unstructured":"Biou, V., Brinkhaus, H., Malenka, R. C. and Matus, A. (2008). Interactions between drebrin and Ras regulate dendritic spine plasticity. Eur. J. Neurosci.27, 2847-2859.","DOI":"10.1111\/j.1460-9568.2008.06269.x"},{"key":"2021042521022693200_REF4","doi-asserted-by":"crossref","unstructured":"Bourne, J. and Harris, K. M. (2007). Do thin spines learn to be mushroom spines that remember? Curr. Opin. Neurobiol.17, 381-386.","DOI":"10.1016\/j.conb.2007.04.009"},{"key":"2021042521022693200_REF5","doi-asserted-by":"crossref","unstructured":"Calon, F., Lim, G. P., Yang, F., Morihara, T., Teter, B., Ubeda, O., Rostaing, P., Triller, A., Salem, N., Jr, Ashe, K. H. et al. (2004). Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron43, 633-645.","DOI":"10.1016\/j.neuron.2004.08.013"},{"key":"2021042521022693200_REF6","doi-asserted-by":"crossref","unstructured":"Chang, E. H., Savage, M. J., Flood, D. G., Thomas, J. M., Levy, R. B., Mahadomrongkul, V., Shirao, T., Aoki, C. and Huerta, P. T. (2006). AMPA receptor downscaling at the onset of Alzheimer's disease pathology in double knockin mice. Proc. Natl. Acad. Sci. USA103, 3410-3415.","DOI":"10.1073\/pnas.0507313103"},{"key":"2021042521022693200_REF7","doi-asserted-by":"crossref","unstructured":"Collin, C., Miyaguchi, K. and Segal, M. (1997). Dendritic spine density and LTP induction in cultured hippocampal slices. J. Neurophysiol.77, 1614-1623.","DOI":"10.1152\/jn.1997.77.3.1614"},{"key":"2021042521022693200_REF8","doi-asserted-by":"crossref","unstructured":"Counts, S. E., Nadeem, M., Lad, S. P., Wuu, J. and Mufson, E. J. (2006). Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment. J. Neuropathol. Exp. Neurol.65, 592-601.","DOI":"10.1097\/00005072-200606000-00007"},{"key":"2021042521022693200_REF9","doi-asserted-by":"crossref","unstructured":"Dailey, M. E. and Smith, S. J. (1996). The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci.16, 2983-2994.","DOI":"10.1523\/JNEUROSCI.16-09-02983.1996"},{"key":"2021042521022693200_REF10","doi-asserted-by":"crossref","unstructured":"Dunaevsky, A., Tashiro, A., Majewska, A., Mason, C. and Yuste, R. (1999). Developmental regulation of spine motility in the mammalian central nervous system. Proc. Natl. Acad. Sci. USA96, 13438-13443.","DOI":"10.1073\/pnas.96.23.13438"},{"key":"2021042521022693200_REF11","doi-asserted-by":"crossref","unstructured":"Engert, F. and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature399, 66-70.","DOI":"10.1038\/19978"},{"key":"2021042521022693200_REF12","doi-asserted-by":"crossref","unstructured":"Fiala, J. C., Feinberg, M., Popov, V. and Harris, K. M. (1998). Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci.18, 8900-8911.","DOI":"10.1523\/JNEUROSCI.18-21-08900.1998"},{"key":"2021042521022693200_REF13","doi-asserted-by":"crossref","unstructured":"Fiala, J. C., Spacek, J. and Harris, K. M. (2002). Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res. Brain Res. Rev.39, 29-54.","DOI":"10.1016\/S0165-0173(02)00158-3"},{"key":"2021042521022693200_REF14","doi-asserted-by":"crossref","unstructured":"Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K. and Inokuchi, K. (2003). Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo.Neuron38, 447-460.","DOI":"10.1016\/S0896-6273(03)00206-X"},{"key":"2021042521022693200_REF15","doi-asserted-by":"crossref","unstructured":"Grutzendler, J., Kasthuri, N. and Gan, W. B. (2002). Long-term dendritic spine stability in the adult cortex. Nature420, 812-816.","DOI":"10.1038\/nature01276"},{"key":"2021042521022693200_REF16","doi-asserted-by":"crossref","unstructured":"Harigaya, Y., Shoji, M., Shirao, T. and Hirai, S. (1996). Disappearance of actin-binding protein, drebrin, from hippocampal synapses in Alzheimer's disease. J. Neurosci. Res.43, 87-92.","DOI":"10.1002\/jnr.490430111"},{"key":"2021042521022693200_REF17","doi-asserted-by":"crossref","unstructured":"Harris, K. M. and Kater, S. B. (1994). Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci.17, 341-371.","DOI":"10.1146\/annurev.ne.17.030194.002013"},{"key":"2021042521022693200_REF18","doi-asserted-by":"crossref","unstructured":"Hasbani, M. J., Schlief, M. L., Fisher, D. A. and Goldberg, M. P. (2001). Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J. Neurosci.21, 2393-2403.","DOI":"10.1523\/JNEUROSCI.21-07-02393.2001"},{"key":"2021042521022693200_REF19","doi-asserted-by":"crossref","unstructured":"Hayashi, K., Ishikawa, R., Ye, L. H., He, X. L., Takata, K., Kohama, K. and Shirao, T. (1996). Modulatory role of drebrin on the cytoskeleton within dendritic spines in the rat cerebral cortex. J. Neurosci.16, 7161-7170.","DOI":"10.1523\/JNEUROSCI.16-22-07161.1996"},{"key":"2021042521022693200_REF20","doi-asserted-by":"crossref","unstructured":"Hayashi, T., Umemori, H., Mishina, M. and Yamamoto, T. (1999). The AMPA receptor interacts with and signals through the protein tyrosine kinase Lyn. Nature397, 72-76.","DOI":"10.1038\/16269"},{"key":"2021042521022693200_REF21","doi-asserted-by":"crossref","unstructured":"Hering, H. and Sheng, M. (2001). Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci.2, 880-888.","DOI":"10.1038\/35104061"},{"key":"2021042521022693200_REF22","doi-asserted-by":"crossref","unstructured":"Honkura, N., Matsuzaki, M., Noguchi, J., Ellis-Davies, G. C. and Kasai, H. (2008). The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron57, 719-729.","DOI":"10.1016\/j.neuron.2008.01.013"},{"key":"2021042521022693200_REF23","doi-asserted-by":"crossref","unstructured":"Ikeda, K., Kaub, P. A., Asada, H., Uyemura, K., Toya, S. and Shirao, T. (1996). Stabilization of adhesion plaques by the expression of drebrin A in fibroblasts. Brain Res. Dev. Brain Res.91, 227-236.","DOI":"10.1016\/0165-3806(95)00181-6"},{"key":"2021042521022693200_REF24","doi-asserted-by":"crossref","unstructured":"Ishikawa, R., Hayashi, K., Shirao, T., Xue, Y., Takagi, T., Sasaki, Y. and Kohama, K. (1994). Drebrin, a development-associated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments. J. Biol. Chem.269, 29928-29933.","DOI":"10.1016\/S0021-9258(18)43970-1"},{"key":"2021042521022693200_REF25","doi-asserted-by":"crossref","unstructured":"Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N. and Nakahara, H. (2003). Structure-stability-function relationships of dendritic spines. Trends Neurosci.26, 360-368.","DOI":"10.1016\/S0166-2236(03)00162-0"},{"key":"2021042521022693200_REF26","doi-asserted-by":"crossref","unstructured":"Kennedy, M. B. (1997). The postsynaptic density at glutamatergic synapses. Trends Neurosci.20, 264-268.","DOI":"10.1016\/S0166-2236(96)01033-8"},{"key":"2021042521022693200_REF27","doi-asserted-by":"crossref","unstructured":"Kim, S. J., Jeon, S., Shin, E. Y., Kim, E. G., Park, J. and Bae, C. D. (2004). AMPA, not NMDA, activates RhoA GTPases and subsequently phosphorylates moesin. Exp. Mol. Med.36, 98-102.","DOI":"10.1038\/emm.2004.14"},{"key":"2021042521022693200_REF28","doi-asserted-by":"crossref","unstructured":"Kobayashi, C., Aoki, C., Kojima, N., Yamazaki, H. and Shirao, T. (2007). Drebrin a content correlates with spine head size in the adult mouse cerebral cortex. J. Comp. Neurol.503, 618-626.","DOI":"10.1002\/cne.21408"},{"key":"2021042521022693200_REF29","doi-asserted-by":"crossref","unstructured":"Mahadomrongkul, V., Huerta, P. T., Shirao, T. and Aoki, C. (2005). Stability of the distribution of spines containing drebrin A in the sensory cortex layer I of mice expressing mutated APP and PS1 genes. Brain Res.1064, 66-74.","DOI":"10.1016\/j.brainres.2005.10.012"},{"key":"2021042521022693200_REF30","doi-asserted-by":"crossref","unstructured":"Maletic-Savatic, M., Malinow, R. and Svoboda, K. (1999). Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science283, 1923-1927.","DOI":"10.1126\/science.283.5409.1923"},{"key":"2021042521022693200_REF31","doi-asserted-by":"crossref","unstructured":"Marrs, G. S., Green, S. H. and Dailey, M. E. (2001). Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat. Neurosci.4, 1006-1013.","DOI":"10.1038\/nn717"},{"key":"2021042521022693200_REF32","doi-asserted-by":"crossref","unstructured":"Mateos, J. M., Luthi, A., Savic, N., Stierli, B., Streit, P., Gahwiler, B. H. and McKinney, R. A. (2007). Synaptic modifications at the CA3-CA1 synapse after chronic AMPA receptor blockade in rat hippocampal slices. J. Physiol.581, 129-138.","DOI":"10.1113\/jphysiol.2006.120550"},{"key":"2021042521022693200_REF33","doi-asserted-by":"crossref","unstructured":"Matsuzaki, M., Ellis-Davies, G. C., Nemoto, T., Miyashita, Y., Iino, M. and Kasai, H. (2001). Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci.4, 1086-1092.","DOI":"10.1038\/nn736"},{"key":"2021042521022693200_REF34","doi-asserted-by":"crossref","unstructured":"Matsuzaki, M., Honkura, N., Ellis-Davies, G. C. and Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature429, 761-766.","DOI":"10.1038\/nature02617"},{"key":"2021042521022693200_REF35","doi-asserted-by":"crossref","unstructured":"Matus, A., Ackermann, M., Pehling, G., Byers, H. R. and Fujiwara, K. (1982). High actin concentrations in brain dendritic spines and postsynaptic densities. Proc. Natl. Acad. Sci. USA79, 7590-7594.","DOI":"10.1073\/pnas.79.23.7590"},{"key":"2021042521022693200_REF36","doi-asserted-by":"crossref","unstructured":"Matus, A., Brinkhaus, H. and Wagner, U. (2000). Actin dynamics in dendritic spines: a form of regulated plasticity at excitatory synapses. Hippocampus10, 555-560.","DOI":"10.1002\/1098-1063(2000)10:5<555::AID-HIPO5>3.0.CO;2-Z"},{"key":"2021042521022693200_REF37","doi-asserted-by":"crossref","unstructured":"McKinney, R. A., Capogna, M., Durr, R., Gahwiler, B. H. and Thompson, S. M. (1999). Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat. Neurosci.2, 44-49.","DOI":"10.1038\/4548"},{"key":"2021042521022693200_REF38","doi-asserted-by":"crossref","unstructured":"Mizui, T., Takahashi, H., Sekino, Y. and Shirao, T. (2005). Overexpression of drebrin A in immature neurons induces the accumulation of F-actin and PSD-95 into dendritic filopodia, and the formation of large abnormal protrusions. Mol. Cell Neurosci.30, 149-157.","DOI":"10.1016\/j.mcn.2005.06.008"},{"key":"2021042521022693200_REF39","doi-asserted-by":"crossref","unstructured":"Noguchi, J., Matsuzaki, M., Ellis-Davies, G. C. and Kasai, H. (2005). Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron46, 609-622.","DOI":"10.1016\/j.neuron.2005.03.015"},{"key":"2021042521022693200_REF40","doi-asserted-by":"crossref","unstructured":"Okamoto, K., Nagai, T., Miyawaki, A. and Hayashi, Y. (2004). Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci.7, 1104-1112.","DOI":"10.1038\/nn1311"},{"key":"2021042521022693200_REF41","doi-asserted-by":"crossref","unstructured":"Papa, M., Bundman, M. C., Greenberger, V. and Segal, M. (1995). Morphological analysis of dendritic spine development in primary cultures of hippocampal neurons. J. Neurosci.15, 1-11.","DOI":"10.1523\/JNEUROSCI.15-01-00001.1995"},{"key":"2021042521022693200_REF42","doi-asserted-by":"crossref","unstructured":"Papa, M. and Segal, M. (1996). Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience71, 1005-1011.","DOI":"10.1016\/0306-4522(95)00490-4"},{"key":"2021042521022693200_REF43","doi-asserted-by":"crossref","unstructured":"Passafaro, M., Nakagawa, T., Sala, C. and Sheng, M. (2003). Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature424, 677-681.","DOI":"10.1038\/nature01781"},{"key":"2021042521022693200_REF44","doi-asserted-by":"crossref","unstructured":"Perez-Otano, I. and Ehlers, M. D. (2005). Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci.28, 229-238.","DOI":"10.1016\/j.tins.2005.03.004"},{"key":"2021042521022693200_REF45","doi-asserted-by":"crossref","unstructured":"Portera-Cailliau, C., Pan, D. T. and Yuste, R. (2003). Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J. Neurosci.23, 7129-7142.","DOI":"10.1523\/JNEUROSCI.23-18-07129.2003"},{"key":"2021042521022693200_REF46","doi-asserted-by":"crossref","unstructured":"Renger, J. J., Egles, C. and Liu, G. (2001). A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron29, 469-484.","DOI":"10.1016\/S0896-6273(01)00219-7"},{"key":"2021042521022693200_REF47","doi-asserted-by":"crossref","unstructured":"Riccio, R. V. and Matthews, M. A. (1985). Effects of intraocular tetrodotoxin on dendritic spines in the developing rat visual cortex: a Golgi analysis. Brain Res.351, 173-182.","DOI":"10.1016\/0165-3806(85)90189-0"},{"key":"2021042521022693200_REF48","doi-asserted-by":"crossref","unstructured":"Saglietti, L., Dequidt, C., Kamieniarz, K., Rousset, M. C., Valnegri, P., Thoumine, O., Beretta, F., Fagni, L., Choquet, D., Sala, C. et al. (2007). Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron54, 461-477.","DOI":"10.1016\/j.neuron.2007.04.012"},{"key":"2021042521022693200_REF49","doi-asserted-by":"crossref","unstructured":"Segal, M. (2005). Dendritic spines and long-term plasticity. Nat. Rev. Neurosci.6, 277-284.","DOI":"10.1038\/nrn1649"},{"key":"2021042521022693200_REF50","doi-asserted-by":"crossref","unstructured":"Sekino, Y., Kojima, N. and Shirao, T. (2007). Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem. Int.51, 92-104.","DOI":"10.1016\/j.neuint.2007.04.029"},{"key":"2021042521022693200_REF51","doi-asserted-by":"crossref","unstructured":"Shim, K. S. and Lubec, G. (2002). Drebrin, a dendritic spine protein, is manifold decreased in brains of patients with Alzheimer's disease and Down syndrome. Neurosci. Lett.324, 209-212.","DOI":"10.1016\/S0304-3940(02)00210-0"},{"key":"2021042521022693200_REF52","doi-asserted-by":"crossref","unstructured":"Shirao, T., Hayashi, K., Ishikawa, R., Isa, K., Asada, H., Ikeda, K. and Uyemura, K. (1994). Formation of thick, curving bundles of actin by drebrin A expressed in fibroblasts. Exp. Cell Res.215, 145-153.","DOI":"10.1006\/excr.1994.1326"},{"key":"2021042521022693200_REF53","doi-asserted-by":"crossref","unstructured":"Star, E. N., Kwiatkowski, D. J. and Murthy, V. N. (2002). Rapid turnover of actin in dendritic spines and its regulation by activity. Nat. Neurosci.5, 239-246.","DOI":"10.1038\/nn811"},{"key":"2021042521022693200_REF54","doi-asserted-by":"crossref","unstructured":"Takahashi, H., Sekino, Y., Tanaka, S., Mizui, T., Kishi, S. and Shirao, T. (2003). Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J. Neurosci.23, 6586-6595.","DOI":"10.1523\/JNEUROSCI.23-16-06586.2003"},{"key":"2021042521022693200_REF55","doi-asserted-by":"crossref","unstructured":"Takahashi, H., Mizui, T. and Shirao, T. (2006). Down-regulation of drebrin A expression suppresses synaptic targeting of NMDA receptors in developing hippocampal neurones. J. Neurochem.97 Suppl. 1, 110-115.","DOI":"10.1111\/j.1471-4159.2005.03536.x"},{"key":"2021042521022693200_REF56","doi-asserted-by":"crossref","unstructured":"Wang, Y. and Durkin, J. P. (1995). alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid, but not N-methyl-D-aspartate, activates mitogen-activated protein kinase through G-protein beta gamma subunits in rat cortical neurons. J. Biol. Chem.270, 22783-22787.","DOI":"10.1074\/jbc.270.39.22783"},{"key":"2021042521022693200_REF57","doi-asserted-by":"crossref","unstructured":"Wang, Y., Small, D. L., Stanimirovic, D. B., Morley, P. and Durkin, J. P. (1997). AMPA receptor-mediated regulation of a Gi-protein in cortical neurons. Nature389, 502-504.","DOI":"10.1038\/39062"},{"key":"2021042521022693200_REF58","doi-asserted-by":"crossref","unstructured":"Yuste, R. and Bonhoeffer, T. (2001). Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci.24, 1071-1089.","DOI":"10.1146\/annurev.neuro.24.1.1071"},{"key":"2021042521022693200_REF59","doi-asserted-by":"crossref","unstructured":"Zhou, Q., Homma, K. J. and Poo, M. M. (2004). Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron44, 749-757.","DOI":"10.1016\/j.neuron.2004.11.011"}],"container-title":["Journal of Cell Science"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/122\/8\/1211\/1376509\/1211.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/122\/8\/1211\/1376509\/1211.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,25]],"date-time":"2021-04-25T21:59:22Z","timestamp":1619387962000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jcs\/article\/122\/8\/1211\/31060\/Activity-of-the-AMPA-receptor-regulates-drebrin"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,4,15]]},"references-count":59,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2009,4,15]]}},"URL":"https:\/\/doi.org\/10.1242\/jcs.043729","relation":{},"ISSN":["1477-9137","0021-9533"],"issn-type":[{"value":"1477-9137","type":"electronic"},{"value":"0021-9533","type":"print"}],"subject":[],"published":{"date-parts":[[2009,4,15]]}}}