{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T22:49:02Z","timestamp":1791413342418,"version":"4.3.3"},"reference-count":82,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,8,17]],"date-time":"2017-08-17T00:00:00Z","timestamp":1502928000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,8,17]],"date-time":"2017-08-17T00:00:00Z","timestamp":1502928000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The brain cytoplasmic (<jats:italic>BC1<\/jats:italic>) RNA is a non-coding RNA (ncRNA) involved in neuronal translational control. Absence of <jats:italic>BC1<\/jats:italic> is associated with altered glutamatergic transmission and maladaptive behavior. Here, we show that pyramidal neurons in the barrel cortex of <jats:italic>BC1<\/jats:italic> knock out (KO) mice display larger excitatory postsynaptic currents and increased spontaneous activity in vivo. Furthermore, <jats:italic>BC1<\/jats:italic> KO mice have enlarged spine heads and postsynaptic densities and increased synaptic levels of glutamate receptors and PSD-95. Of note, <jats:italic>BC1<\/jats:italic> KO mice show aberrant structural plasticity in response to whisker deprivation, impaired texture novel object recognition and altered social behavior. Thus, our study highlights a role for <jats:italic>BC1<\/jats:italic> RNA in experience-dependent plasticity and learning in the mammalian adult neocortex, and provides insight into the function of brain ncRNAs regulating synaptic transmission, plasticity and behavior, with potential relevance in the context of intellectual disabilities and psychiatric disorders.<\/jats:p>","DOI":"10.1038\/s41467-017-00311-2","type":"journal-article","created":{"date-parts":[[2017,8,10]],"date-time":"2017-08-10T16:42:03Z","timestamp":1502383323000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":68,"title":["The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning"],"prefix":"10.1038","volume":"8","author":[{"given":"Victor","family":"Briz","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3709-5504","authenticated-orcid":false,"given":"Leonardo","family":"Restivo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emanuela","family":"Pasciuto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Konrad","family":"Juczewski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valentina","family":"Mercaldo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9104-5949","authenticated-orcid":false,"given":"Adrian C.","family":"Lo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pieter","family":"Baatsen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia V.","family":"Gounko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonella","family":"Borreca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tiziana","family":"Girardi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rossella","family":"Luca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julie","family":"Nys","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rogier B.","family":"Poorthuis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1365-5340","authenticated-orcid":false,"given":"Huibert D.","family":"Mansvelder","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gilberto","family":"Fisone","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martine","family":"Ammassari-Teule","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lutgarde","family":"Arckens","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrik","family":"Krieger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0228-4169","authenticated-orcid":false,"given":"Rhiannon","family":"Meredith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4419-210X","authenticated-orcid":false,"given":"Claudia","family":"Bagni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,8,17]]},"reference":[{"key":"311_CR1","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1038\/nrn2763","volume":"10","author":"G Schratt","year":"2009","unstructured":"Schratt, G. microRNAs at the synapse. Nat. Rev. Neurosci. \n                           10, 842\u2013849 (2009).","journal-title":"Nat. Rev. Neurosci."},{"key":"311_CR2","doi-asserted-by":"publisher","first-page":"861","DOI":"10.1016\/j.neuron.2015.09.045","volume":"88","author":"JA Briggs","year":"2015","unstructured":"Briggs, J. A., Wolvetang, E. J., Mattick, J. S., Rinn, J. L. & Barry, G. Mechanisms of long non-coding RNAs in mammalian nervous system development, plasticity, disease, and evolution. Neuron. \n                           88, 861\u2013877 (2015).","journal-title":"Neuron."},{"key":"311_CR3","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1016\/j.mrrev.2015.08.002","volume":"766","author":"P Sosi\u0144ska","year":"2015","unstructured":"Sosi\u0144ska, P., Miku\u0142a-Pietrasik, J. & Ksi\u0105\u017cek, K. The double-edged sword of long non-coding RNA: the role of human brain-specific BC200 RNA in translational control, neurodegenerative diseases, and cancer. Mutat. Res. Rev. Mutat. Res. \n                           766, 58\u201367 (2015).","journal-title":"Mutat. Res. Rev. Mutat. Res."},{"key":"311_CR4","doi-asserted-by":"publisher","first-page":"9977","DOI":"10.1523\/JNEUROSCI.3893-08.2009","volume":"29","author":"J Zhong","year":"2009","unstructured":"Zhong, J. et al. BC1 regulation of metabotropic glutamate receptor-mediated neuronal excitability. J. Neurosci. \n                           29, 9977\u20139986 (2009).","journal-title":"J. Neurosci."},{"key":"311_CR5","doi-asserted-by":"publisher","first-page":"e15509","DOI":"10.1371\/journal.pone.0015509","volume":"5","author":"J Zhong","year":"2010","unstructured":"Zhong, J. et al. Regulatory BC1 RNA and the fragile X mental retardation protein: convergent functionality in brain. PLoS ONE \n                           5, e15509 (2010).","journal-title":"PLoS ONE"},{"key":"311_CR6","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/j.bbr.2004.02.015","volume":"154","author":"L Lewejohann","year":"2004","unstructured":"Lewejohann, L. et al. Role of a neuronal small non-messenger RNA: behavioural alterations in BC1 RNA-deleted mice. Behav. Brain. Res. \n                           154, 273\u2013289 (2004).","journal-title":"Behav. Brain. Res."},{"key":"311_CR7","doi-asserted-by":"publisher","first-page":"4942","DOI":"10.1073\/pnas.79.16.4942","volume":"79","author":"JG Sutcliffe","year":"1982","unstructured":"Sutcliffe, J. G., Milner, R. J., Bloom, F. E. & Lerner, R. A. Common 82-nucleotide sequence unique to brain RNA. Proc. Natl Acad. Sci. USA \n                           79, 4942\u20134946 (1982).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"311_CR8","doi-asserted-by":"publisher","first-page":"28300","DOI":"10.1038\/srep28300","volume":"6","author":"T Robeck","year":"2016","unstructured":"Robeck, T. et al. BC1 RNA motifs required for dendritic transport in vivo. Sci. Rep. \n                           6, 28300 (2016).","journal-title":"Sci. Rep."},{"key":"311_CR9","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1016\/j.biopsych.2007.09.008","volume":"63","author":"D Centonze","year":"2008","unstructured":"Centonze, D. et al. Abnormal striatal GABA transmission in the mouse model for the fragile X syndrome. Biol. Psychiatry \n                           63, 963\u2013973 (2008).","journal-title":"Biol. Psychiatry"},{"key":"311_CR10","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1016\/j.mcn.2006.11.015","volume":"34","author":"F Ferrari","year":"2007","unstructured":"Ferrari, F. et al. The fragile X mental retardation protein-RNP granules show an mGluR-dependent localization in the post-synaptic spines. Mol. Cell. Neurosci. \n                           34, 343\u2013354 (2007).","journal-title":"Mol. Cell. Neurosci."},{"key":"311_CR11","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1016\/S0092-8674(03)00079-5","volume":"112","author":"F Zalfa","year":"2003","unstructured":"Zalfa, F. et al. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell \n                           112, 317\u2013327 (2003).","journal-title":"Cell"},{"key":"311_CR12","doi-asserted-by":"publisher","first-page":"33403","DOI":"10.1074\/jbc.M504286200","volume":"280","author":"F Zalfa","year":"2005","unstructured":"Zalfa, F. et al. Fragile X mental retardation protein (FMRP) binds specifically to the brain cytoplasmic RNAs BC1\/BC200 via a novel RNA-binding motif. J. Biol. Chem. \n                           280, 33403\u201333410 (2005).","journal-title":"J. Biol. Chem."},{"key":"311_CR13","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1016\/S0022-2836(02)00655-1","volume":"321","author":"R Muddashetty","year":"2002","unstructured":"Muddashetty, R. et al. Poly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles. J. Mol. Biol. \n                           321, 433\u2013445 (2002).","journal-title":"J. Mol. Biol."},{"key":"311_CR14","doi-asserted-by":"crossref","first-page":"10232","DOI":"10.1523\/JNEUROSCI.22-23-10232.2002","volume":"22","author":"H Wang","year":"2002","unstructured":"Wang, H. et al. Dendritic BC1 RNA: functional role in regulation of translation initiation. J. Neurosci. \n                           22, 10232\u201310241 (2002).","journal-title":"J. Neurosci."},{"key":"311_CR15","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1083\/jcb.201401005","volume":"207","author":"T Eom","year":"2014","unstructured":"Eom, T. et al. Neuronal BC RNAs cooperate with eIF4B to mediate activity-dependent translational control. J. Cell. Biol. \n                           207, 237\u2013252 (2014).","journal-title":"J. Cell. Biol."},{"key":"311_CR16","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.1016\/j.cell.2008.07.031","volume":"134","author":"I Napoli","year":"2008","unstructured":"Napoli, I. et al. The Fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell \n                           134, 1042\u20131054 (2008).","journal-title":"Cell"},{"key":"311_CR17","doi-asserted-by":"publisher","first-page":"4086","DOI":"10.1093\/nar\/gkr1254","volume":"40","author":"C Lacoux","year":"2012","unstructured":"Lacoux, C. et al. BC1-FMRP interaction is modulated by 2\u2032-O-methylation: RNA-binding activity of the tudor domain and translational regulation at synapses. Nucleic Acids Res. \n                           40, 4086\u20134096 (2012).","journal-title":"Nucleic Acids Res."},{"key":"311_CR18","doi-asserted-by":"publisher","first-page":"14","DOI":"10.3389\/neuro.04.014.2009","volume":"3","author":"RS Zukin","year":"2009","unstructured":"Zukin, R. S., Richter, J. D. & Bagni, C. Signals, synapses, and synthesis: how new proteins control plasticity. Front. Neural Circuits \n                           3, 14 (2009).","journal-title":"Front. Neural Circuits"},{"key":"311_CR19","doi-asserted-by":"publisher","first-page":"6435","DOI":"10.1128\/MCB.23.18.6435-6441.2003","volume":"23","author":"BV Skryabin","year":"2003","unstructured":"Skryabin, B. V. et al. Neuronal untranslated BC1 RNA: targeted gene elimination in mice. Mol. Cell. Biol. \n                           23, 6435\u20136441 (2003).","journal-title":"Mol. Cell. Biol."},{"key":"311_CR20","doi-asserted-by":"publisher","first-page":"8885","DOI":"10.1523\/JNEUROSCI.0548-07.2007","volume":"27","author":"D Centonze","year":"2007","unstructured":"Centonze, D. et al. The brain cytoplasmic RNA BC1 regulates dopamine D2 receptor-mediated transmission in the striatum. J. Neurosci. \n                           27, 8885\u20138892 (2007).","journal-title":"J. Neurosci."},{"key":"311_CR21","doi-asserted-by":"publisher","first-page":"1500","DOI":"10.1038\/npp.2010.19","volume":"35","author":"M Maccarrone","year":"2010","unstructured":"Maccarrone, M. et al. Abnormal mGlu 5 receptor\/endocannabinoid coupling in mice lacking FMRP and BC1 RNA. Neuropsychopharmacology \n                           35, 1500\u20131509 (2010).","journal-title":"Neuropsychopharmacology"},{"key":"311_CR22","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1016\/j.neuron.2007.09.017","volume":"56","author":"CCH Petersen","year":"2007","unstructured":"Petersen, C. C. H. The functional organization of the barrel cortex. Neuron \n                           56, 339\u2013355 (2007).","journal-title":"Neuron"},{"key":"311_CR23","doi-asserted-by":"publisher","first-page":"e374","DOI":"10.1038\/tp.2014.16","volume":"4","author":"M Pathania","year":"2014","unstructured":"Pathania, M. et al. The autism and schizophrenia associated gene CYFIP1 is critical for the maintenance of dendritic complexity and the stabilization of mature spines. Transl. Psychiatry \n                           4, e374 (2014).","journal-title":"Transl. Psychiatry"},{"key":"311_CR24","doi-asserted-by":"publisher","first-page":"11557","DOI":"10.1073\/pnas.0504984102","volume":"102","author":"L Restivo","year":"2005","unstructured":"Restivo, L. et al. Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proc. Natl Acad. Sci. USA \n                           102, 11557\u201311562 (2005).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"311_CR25","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/S0165-0173(02)00158-3","volume":"39","author":"JC Fiala","year":"2002","unstructured":"Fiala, J. C., Spacek, J. & Harris, K. M. Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res. Brain Res. Rev. \n                           39, 29\u201354 (2002).","journal-title":"Brain Res. Brain Res. Rev."},{"key":"311_CR26","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1002\/dneu.22417","volume":"77","author":"V Mart\u00ednez-Cerde\u00f1","year":"2017","unstructured":"Martinez-Cerdeno, V. Dendrite and spine modifications in autism and related neurodevelopmental disorders in patients and animal models. Dev. Neurobiol. \n                           77, 393\u2013404 (2017).","journal-title":"Dev. Neurobiol."},{"key":"311_CR27","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.1038\/mp.2014.124","volume":"20","author":"A Oguro-Ando","year":"2014","unstructured":"Oguro-Ando, A. et al. Increased CYFIP1 dosage alters cellular and dendritic morphology and dysregulates mTOR. Mol. Psychiatry \n                           20, 1069\u20131078 (2014).","journal-title":"Mol. Psychiatry"},{"key":"311_CR28","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1007\/978-3-7091-0932-8_23","volume":"970","author":"S De Rubeis","year":"2012","unstructured":"De Rubeis, S., Fern\u00e1ndez, E., Buzzi, A., Di Marino, D. & Bagni, C. Molecular and cellular aspects of mental retardation in the Fragile X syndrome: from gene mutation\/s to spine dysmorphogenesis. Adv. Exp. Med. Biol. \n                           970, 517\u2013551 (2012).","journal-title":"Adv. Exp. Med. Biol."},{"key":"311_CR29","doi-asserted-by":"crossref","first-page":"6819","DOI":"10.1523\/JNEUROSCI.22-15-06819.2002","volume":"22","author":"IE Brown","year":"2002","unstructured":"Brown, I. E. & Bower, J. M. The influence of somatosensory cortex on climbing fiber responses in the lateral hemispheres of the rat cerebellum after peripheral tactile stimulation. J. Neurosci. \n                           22, 6819\u20136829 (2002).","journal-title":"J. Neurosci."},{"key":"311_CR30","doi-asserted-by":"publisher","first-page":"1477","DOI":"10.1016\/j.neuron.2013.10.059","volume":"80","author":"T Yamashita","year":"2013","unstructured":"Yamashita, T. et al. Membrane potential dynamics of neocortical projection neurons driving target-specific signals. Neuron \n                           80, 1477\u20131490 (2013).","journal-title":"Neuron"},{"key":"311_CR31","doi-asserted-by":"publisher","first-page":"381","DOI":"10.3389\/fncel.2014.00381","volume":"8","author":"JG Hanley","year":"2014","unstructured":"Hanley, J. G. Actin-dependent mechanisms in AMPA receptor trafficking. Front. Cell. Neurosci. \n                           8, 381 (2014).","journal-title":"Front. Cell. Neurosci."},{"key":"311_CR32","doi-asserted-by":"publisher","first-page":"5338","DOI":"10.1523\/JNEUROSCI.0937-07.2007","volume":"27","author":"RS Muddashetty","year":"2007","unstructured":"Muddashetty, R. S., Keli\u0107, S., Gross, C., Xu, M. & Bassell, G. J. Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J. Neurosci. \n                           27, 5338\u20135348 (2007).","journal-title":"J. Neurosci."},{"key":"311_CR33","doi-asserted-by":"publisher","first-page":"3222","DOI":"10.1039\/C5MB00423C","volume":"11","author":"S Stefanovic","year":"2015","unstructured":"Stefanovic, S. et al. Fragile X mental retardation protein interactions with a G quadruplex structure in the 3\u2032-untranslated region of NR2B mRNA. Mol. Biosyst. \n                           11, 3222\u20133230 (2015).","journal-title":"Mol. Biosyst."},{"key":"311_CR34","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1074\/jbc.274.1.151","volume":"274","author":"KH Huh","year":"1999","unstructured":"Huh, K. H. & Wenthold, R. J. Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J. Biol. Chem. \n                           274, 151\u2013157 (1999).","journal-title":"J. Biol. Chem."},{"key":"311_CR35","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1038\/nmeth.1314","volume":"6","author":"EK Schmidt","year":"2009","unstructured":"Schmidt, E. K., Clavarino, G., Ceppi, M. & Pierre, P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat. Methods \n                           6, 275\u2013277 (2009).","journal-title":"Nat. Methods"},{"key":"311_CR36","doi-asserted-by":"publisher","first-page":"2269","DOI":"10.1523\/JNEUROSCI.2302-14.2015","volume":"35","author":"V Briz","year":"2015","unstructured":"Briz, V. et al. Activity-dependent rapid local RhoA synthesis is required for hippocampal synaptic plasticity. J. Neurosci. \n                           35, 2269\u20132282 (2015).","journal-title":"J. Neurosci."},{"key":"311_CR37","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1111\/jnc.13723","volume":"139","author":"SR Louros","year":"2016","unstructured":"Louros, S. R. & Osterweil, E. K. Perturbed proteostasis in autism spectrum disorders. J. Neurochem. \n                           139, 1081\u20131092 (2016).","journal-title":"J. Neurochem."},{"key":"311_CR38","doi-asserted-by":"publisher","first-page":"4155","DOI":"10.1523\/JNEUROSCI.0175-06.2006","volume":"26","author":"KJ Bender","year":"2006","unstructured":"Bender, K. J., Allen, C. B., Bender, V. A. & Feldman, D. E. Synaptic basis for whisker deprivation-induced synaptic depression in rat somatosensory cortex. J. Neurosci. \n                           26, 4155\u20134165 (2006).","journal-title":"J. Neurosci."},{"key":"311_CR39","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1038\/nn1012","volume":"6","author":"CB Allen","year":"2003","unstructured":"Allen, C. B., Celikel, T. & Feldman, D. E. Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat. Neurosci. \n                           6, 291\u2013299 (2003).","journal-title":"Nat. Neurosci."},{"key":"311_CR40","doi-asserted-by":"publisher","first-page":"2082","DOI":"10.1073\/pnas.90.5.2082","volume":"90","author":"ME Diamond","year":"1993","unstructured":"Diamond, M. E., Armstrong-James, M. & Ebner, F. F. Experience-dependent plasticity in adult rat barrel cortex. Proc. Natl Acad. Sci. USA \n                           90, 2082\u20132086 (1993).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"311_CR41","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1002\/(SICI)1096-9861(19981012)400:1<110::AID-CNE8>3.0.CO;2-C","volume":"400","author":"AM Vees","year":"1998","unstructured":"Vees, A. M., Micheva, K. D., Beaulieu, C. & Descarries, L. Increased number and size of dendritic spines in ipsilateral barrel field cortex following unilateral whisker trimming in postnatal rat. J. Comp. Neurol. \n                           400, 110\u2013124 (1998).","journal-title":"J. Comp. Neurol."},{"key":"311_CR42","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/j.bbr.2012.10.022","volume":"238","author":"Y-F Chu","year":"2013","unstructured":"Chu, Y.-F., Yen, C.-T. & Lee, L.-J. Neonatal whisker clipping alters behavior, neuronal structure and neural activity in adult rats. Behav. Brain Res. \n                           238, 124\u2013133 (2013).","journal-title":"Behav. Brain Res."},{"key":"311_CR43","doi-asserted-by":"publisher","first-page":"E726","DOI":"10.1073\/pnas.1300424110","volume":"110","author":"MT Butko","year":"2013","unstructured":"Butko, M. T. et al. In vivo quantitative proteomics of somatosensory cortical synapses shows which protein levels are modulated by sensory deprivation. Proc. Natl Acad. Sci. USA \n                           110, E726\u2013E735 (2013).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"311_CR44","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1016\/j.bbr.2013.12.027","volume":"261","author":"M Liguz-Lecznar","year":"2014","unstructured":"Liguz-Lecznar, M., Zakrzewska, R., Daniszewska, K. & Kossut, M. Functional assessment of sensory functions after photothrombotic stroke in the barrel field of mice. Behav. Brain Res. \n                           261, 202\u2013209 (2014).","journal-title":"Behav. Brain Res."},{"key":"311_CR45","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1016\/j.bbr.2008.12.028","volume":"199","author":"D Lapray","year":"2009","unstructured":"Lapray, D., Bergeler, J. & Luhmann, H. J. Stimulus-induced gamma activity in the electrocorticogram of freely moving rats: the neuronal signature of novelty detection. Behav. Brain Res. \n                           199, 350\u2013354 (2009).","journal-title":"Behav. Brain Res."},{"key":"311_CR46","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1016\/j.cell.2016.05.033","volume":"166","author":"LLL Orefice","year":"2016","unstructured":"Orefice, L. L. L. et al. Peripheral mechanosensory neuron dysfunction underlies tactile and behavioral deficits in mouse models of ASDs. Cell \n                           166, 299\u2013314 (2016).","journal-title":"Cell"},{"key":"311_CR47","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/j.bbr.2014.08.002","volume":"285","author":"SJ Cohen","year":"2015","unstructured":"Cohen, S. J. & Stackman, R. W. Assessing rodent hippocampal involvement in the novel object recognition task. A review. Behav. Brain Res. \n                           285, 105\u2013117 (2015).","journal-title":"Behav. Brain Res."},{"key":"311_CR48","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/j.nlm.2015.07.013","volume":"124","author":"E Pasciuto","year":"2015","unstructured":"Pasciuto, E. et al. Autism spectrum disorders: translating human deficits into mouse behavior. Neurobiol. Learn Mem. \n                           124, 71\u201387 (2015).","journal-title":"Neurobiol. Learn Mem."},{"key":"311_CR49","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1101\/lm.035956.114","volume":"21","author":"AR Santos","year":"2014","unstructured":"Santos, A. R., Kanellopoulos, A. K. & Bagni, C. Learning and behavioral deficits associated with the absence of the fragile X mental retardation protein: what a fly and mouse model can teach us. Learn. Mem. \n                           21, 543\u2013555 (2014).","journal-title":"Learn. Mem."},{"key":"311_CR50","doi-asserted-by":"publisher","first-page":"12001","DOI":"10.1523\/JNEUROSCI.1663-14.2014","volume":"34","author":"H Arakawa","year":"2014","unstructured":"Arakawa, H. et al. Thalamic NMDA receptor function is necessary for patterning of the thalamocortical somatosensory map and for sensorimotor behaviors. J. Neurosci. \n                           34, 12001\u201312014 (2014).","journal-title":"J. Neurosci."},{"key":"311_CR51","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1016\/j.neuron.2015.06.032","volume":"87","author":"E Pasciuto","year":"2015","unstructured":"Pasciuto, E. et al. Dysregulated ADAM10-mediated processing of APP during a critical time window leads to synaptic deficits in fragile X syndrome. Neuron \n                           87, 382\u2013398 (2015).","journal-title":"Neuron"},{"key":"311_CR52","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1093\/cercor\/10.10.981","volume":"10","author":"WE Kaufmann","year":"2000","unstructured":"Kaufmann, W. E. & Moser, H. W. Dendritic anomalies in disorders associated with mental retardation. Cereb. Cortex \n                           10, 981\u2013991 (2000).","journal-title":"Cereb. Cortex"},{"key":"311_CR53","doi-asserted-by":"publisher","first-page":"1169","DOI":"10.1016\/j.neuron.2013.06.039","volume":"79","author":"S DeRubeis","year":"2013","unstructured":"DeRubeis, S. et al. CYFIP1 coordinates mRNA translation and cytoskeleton remodeling to ensure proper dendritic Spine formation. Neuron \n                           79, 1169\u20131182 (2013).","journal-title":"Neuron"},{"key":"311_CR54","doi-asserted-by":"publisher","first-page":"5938","DOI":"10.1523\/JNEUROSCI.1547-09.2009","volume":"29","author":"NP Belichenko","year":"2009","unstructured":"Belichenko, N. P. et al. The \u2018Down syndrome critical region\u2019 is sufficient in the mouse model to confer behavioral, neurophysiological, and synaptic phenotypes characteristic of Down syndrome. J. Neurosci. \n                           29, 5938\u20135948 (2009).","journal-title":"J. Neurosci."},{"key":"311_CR55","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1002\/jnr.20806","volume":"83","author":"EM Johnson","year":"2006","unstructured":"Johnson, E. M. et al. Role of Pur alpha in targeting mRNA to sites of translation in hippocampal neuronal dendrites. J. Neurosci. Res. \n                           83, 929\u2013943 (2006).","journal-title":"J. Neurosci. Res."},{"key":"311_CR56","doi-asserted-by":"publisher","first-page":"3008","DOI":"10.1128\/MCB.01800-07","volume":"28","author":"D Lin","year":"2008","unstructured":"Lin, D., Pestova, T. V., Hellen, C. U. T. & Tiedge, H. Translational control by a small RNA: dendritic BC1 RNA targets the eukaryotic initiation factor 4A helicase mechanism. Mol. Cell. Biol. \n                           28, 3008\u20133019 (2008).","journal-title":"Mol. Cell. Biol."},{"key":"311_CR57","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1126\/science.290.5495.1364","volume":"290","author":"AE El-Husseini","year":"2000","unstructured":"El-Husseini, A. E., Schnell, E., Chetkovich, D. M., Nicoll, R. A. & Bredt, D. S. PSD-95 involvement in maturation of excitatory synapses. Science \n                           290, 1364\u20131368 (2000).","journal-title":"Science"},{"key":"311_CR58","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1016\/S0896-6273(02)00785-7","volume":"35","author":"LE Ostroff","year":"2002","unstructured":"Ostroff, L. E., Fiala, J. C., Allwardt, B. & Harris, K. M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron \n                           35, 535\u2013545 (2002).","journal-title":"Neuron"},{"key":"311_CR59","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1093\/cercor\/bhm041","volume":"18","author":"M De Roo","year":"2008","unstructured":"De Roo, M., Klauser, P., Mendez, P., Poglia, L. & Muller, D. Activity-dependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cereb. Cortex \n                           18, 151\u2013161 (2008).","journal-title":"Cereb. Cortex"},{"key":"311_CR60","doi-asserted-by":"publisher","first-page":"14437","DOI":"10.1073\/pnas.1009268107","volume":"107","author":"HJ Pi","year":"2010","unstructured":"Pi, H. J. et al. CaMKII control of spine size and synaptic strength: role of phosphorylation states and nonenzymatic action. Proc. Natl Acad. Sci. USA \n                           107, 14437\u201314442 (2010).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"311_CR61","doi-asserted-by":"publisher","first-page":"7116","DOI":"10.1523\/JNEUROSCI.2802-14.2015","volume":"35","author":"MF Ifrim","year":"2015","unstructured":"Ifrim, M. F., Williams, K. R. & Bassell, G. J. Single-molecule imaging of PSD-95 mRNA translation in dendrites and its dysregulation in a mouse model of fragile X syndrome. J. Neurosci. \n                           35, 7116\u20137130 (2015).","journal-title":"J. Neurosci."},{"key":"311_CR62","doi-asserted-by":"publisher","first-page":"9402","DOI":"10.1523\/JNEUROSCI.4800-14.2015","volume":"35","author":"E Fern\u00e1ndez","year":"2015","unstructured":"Fern\u00e1ndez, E. et al. FXR2P exerts a positive translational control and is required for the activity-dependent increase of PSD95 expression. J. Neurosci. \n                           35, 9402\u20139408 (2015).","journal-title":"J. Neurosci."},{"key":"311_CR63","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1038\/nn1893","volume":"10","author":"F Zalfa","year":"2007","unstructured":"Zalfa, F. et al. A new function for the fragile X mental retardation protein in regulation of PSD-95 mRNA stability. Nat. Neurosci. \n                           10, 578\u2013587 (2007).","journal-title":"Nat. Neurosci."},{"key":"311_CR64","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.mcn.2009.09.013","volume":"43","author":"S De Rubeis","year":"2010","unstructured":"De Rubeis, S. & Bagni, C. Fragile X mental retardation protein control of neuronal mRNA metabolism: insights into mRNA stability. Mol. Cell. Neurosci. \n                           43, 43\u201350 (2010).","journal-title":"Mol. Cell. Neurosci."},{"key":"311_CR65","doi-asserted-by":"publisher","first-page":"e39585","DOI":"10.1371\/journal.pone.0039585","volume":"7","author":"S Standley","year":"2012","unstructured":"Standley, S. et al. Trafficking of the NMDAR2B receptor subunit distal cytoplasmic tail from endoplasmic reticulum to the synapse. PLoS ONE \n                           7, e39585 (2012).","journal-title":"PLoS ONE"},{"key":"311_CR66","doi-asserted-by":"publisher","first-page":"10138","DOI":"10.1523\/JNEUROSCI.3159-04.2004","volume":"24","author":"Y Lin","year":"2004","unstructured":"Lin, Y., Skeberdis, V. A., Francesconi, A., Bennett, M. V. L. & Zukin, R. S. Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J. Neurosci. \n                           24, 10138\u201310148 (2004).","journal-title":"J. Neurosci."},{"key":"311_CR67","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1038\/nrn3192","volume":"13","author":"J Lisman","year":"2012","unstructured":"Lisman, J., Yasuda, R. & Raghavachari, S. Mechanisms of CaMKII action in long-term potentiation. Nat. Rev. Neurosci. \n                           13, 169\u2013182 (2012).","journal-title":"Nat. Rev. Neurosci."},{"key":"311_CR68","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1146\/annurev.neuro.30.051606.094222","volume":"30","author":"VA Alvarez","year":"2007","unstructured":"Alvarez, V. A. & Sabatini, B. L. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. \n                           30, 79\u201397 (2007).","journal-title":"Annu. Rev. Neurosci."},{"key":"311_CR69","doi-asserted-by":"publisher","first-page":"1334","DOI":"10.1073\/pnas.0335785100","volume":"100","author":"A Yoshii","year":"2003","unstructured":"Yoshii, A., Sheng, M. H. & Constantine-Paton, M. Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons. Proc. Natl Acad. Sci USA \n                           100, 1334\u20131339 (2003).","journal-title":"Proc. Natl Acad. Sci USA"},{"key":"311_CR70","doi-asserted-by":"publisher","first-page":"1590","DOI":"10.1046\/j.1471-4159.2000.0751590.x","volume":"75","author":"H Hoffmann","year":"2002","unstructured":"Hoffmann, H., Gremme, T., Hatt, H. & Gottmann, K. Synaptic activity-dependent developmental regulation of NMDA receptor subunit expression in cultured neocortical neurons. J. Neurochem. \n                           75, 1590\u20131599 (2002).","journal-title":"J. Neurochem."},{"key":"311_CR71","doi-asserted-by":"publisher","first-page":"1281","DOI":"10.1111\/j.1460-9568.2012.08044.x","volume":"35","author":"S Jaffer","year":"2012","unstructured":"Jaffer, S., Vorobyov, V., Kind, P. C. & Sengpiel, F. Experience-dependent regulation of functional maps and synaptic protein expression in the cat visual cortex. Eur. J. Neurosci. \n                           35, 1281\u20131294 (2012).","journal-title":"Eur. J. Neurosci."},{"key":"311_CR72","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/S0896-6273(01)00187-8","volume":"29","author":"BD Philpot","year":"2001","unstructured":"Philpot, B. D., Sekhar, A. K., Shouval, H. Z. & Bear, M. F. Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron \n                           29, 157\u2013169 (2001).","journal-title":"Neuron"},{"key":"311_CR73","doi-asserted-by":"publisher","first-page":"17768","DOI":"10.1073\/pnas.1012496107","volume":"107","author":"F Pan","year":"2010","unstructured":"Pan, F., Aldridge, G. M., Greenough, W. T. & Gan, W.-B. Dendritic spine instability and insensitivity to modulation by sensory experience in a mouse model of fragile X syndrome. Proc. Natl Acad. Sci. USA \n                           107, 17768\u201317773 (2010).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"311_CR74","doi-asserted-by":"publisher","first-page":"1581","DOI":"10.1016\/j.cell.2012.11.040","volume":"151","author":"N-P Tsai","year":"2012","unstructured":"Tsai, N.-P. et al. Multiple autism-linked genes mediate synapse elimination via proteasomal degradation of a synaptic scaffold PSD-95. Cell \n                           151, 1581\u20131594 (2012).","journal-title":"Cell"},{"key":"311_CR75","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1016\/j.bbr.2012.09.044","volume":"237","author":"HPP Wu","year":"2013","unstructured":"Wu, H. P. P., Ioffe, J. C., Iverson, M. M., Boon, J. M. & Dyck, R. H. Novel, whisker-dependent texture discrimination task for mice. Behav. Brain Res. \n                           237, 238\u2013242 (2013).","journal-title":"Behav. Brain Res."},{"key":"311_CR76","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.nbd.2016.09.007","volume":"96","author":"K Juczewski","year":"2016","unstructured":"Juczewski, K. et al. Somatosensory map expansion and altered processing of tactile inputs in a mouse model of fragile X syndrome. Neurobiol. Dis. \n                           96, 201\u2013215 (2016).","journal-title":"Neurobiol. Dis."},{"key":"311_CR77","first-page":"229","volume":"174","author":"CH Horner","year":"1991","unstructured":"Horner, C. H., O\u2019Regan, M. & Arbuthnott, E. Neural plasticity of the hippocampal (CA1) pyramidal cell--quantitative changes in spine density following handling and injection for drug testing. J. Anat. \n                           174, 229\u2013238 (1991).","journal-title":"J. Anat."},{"key":"311_CR78","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/0165-0270(88)90114-8","volume":"25","author":"K Horikawa","year":"1988","unstructured":"Horikawa, K. & Armstrong, W. E. A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J. Neurosci. Methods \n                           25, 1\u201311 (1988).","journal-title":"J. Neurosci. Methods"},{"key":"311_CR79","doi-asserted-by":"crossref","unstructured":"Ruszczycki, B. et al. Sampling issues in quantitative analysis of dendritic spines morphology. BMC Bioinform. https:\/\/dx.doi.org\/10.1186\/1471-2105-13-213 (2012).","DOI":"10.1186\/1471-2105-13-213"},{"key":"311_CR80","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fendo.2014.00022","volume":"5","author":"V Briz","year":"2014","unstructured":"Briz, V. & Baudry, M. Estrogen regulates protein synthesis and actin polymerization in hippocampal neurons through different molecular mechanisms. Front. Endocrinol. (Lausanne) \n                           5, 1\u201314 (2014).","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"311_CR81","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/j.nbd.2014.12.021","volume":"75","author":"CEF de Esch","year":"2015","unstructured":"de Esch, C. E. F. et al. Fragile X mice have robust mGluR5-dependent alterations of social behaviour in the automated tube test. Neurobiol. Dis. \n                           75, 31\u201339 (2015).","journal-title":"Neurobiol. Dis."},{"key":"311_CR82","doi-asserted-by":"crossref","unstructured":"Williams, R. W. in Mouse Brain Development (Goffinet, A.F., Rakic, P., eds) 21\u201349 (Springer, 2000).","DOI":"10.1007\/978-3-540-48002-0_2"}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-00311-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-00311-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-00311-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,22]],"date-time":"2022-12-22T19:48:23Z","timestamp":1671738503000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41467-017-00311-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,8,17]]},"references-count":82,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["311"],"URL":"https:\/\/doi.org\/10.1038\/s41467-017-00311-2","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,8,17]]},"assertion":[{"value":"5 August 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 June 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 August 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"293"}}