Visual cortical circuits show profound plasticity during early life and are later stabilized by molecular "brakes" limiting excessive rewiring beyond a critical period. The mechanisms coordinating the expression of these factors during the transition from development to adulthood remain unknown. We found that miR-29a expression in the visual cortex dramatically increases with age, but it is not experience-dependent. Precocious high levels of miR-29a blocked ocular dominance plasticity and caused an early appearance of perineuronal nets. Conversely, inhibition of miR-29a in adult mice using LNA antagomirs activated ocular dominance plasticity, reduced perineuronal nets, and restored their juvenile chemical composition. Activated adult plasticity had the typical functional and proteomic signature of critical period plasticity. Transcriptomic and proteomic studies indicated that miR-29a manipulation regulates the expression of plasticity brakes in specific cortical circuits. These data indicate that miR-29a is a regulator of the plasticity brakes promoting age-dependent stabilization of visual cortical connections.

Department of Clinical and Experimental Medicine University of Pisa Pisa Italy

Department of Developmental Neuroscience IRCCS Stella Maris Foundation Pisa Italy

Department of Neuroscience Psychology Drug Research and Child Health NEUROFARBA University of Florence Florence Italy

Department of Translational Research and New Technologies in Medicine and Surgery University of Pisa Pisa Italy

Institute for Genomics and Bioinformatics School of Information and Computer Sciences University of California Irvine CA USA

Institute of Experimental Medicine Czech Academy of Science Prague Czech Republic

Institute of Neuroscience National Research Council Pisa Italy

Lab Scuola Normale Superiore Pisa Italy

Leibniz Institute on Aging Fritz Lipmann Institute Jena Germany

School of Biomedical Sciences University of Leeds Leeds UK

Stazione Zoologica Anton Dohrn Naples Italy

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Amodio N, Rossi M, Raimondi L, Pitari MR, Botta C, Tagliaferri P, Tassone P (2015) miR‐29s: a family of epi‐miRNAs with therapeutic implications in hematologic malignancies. Oncotarget 6: 12837–12861 PubMed PMC

Apulei J, Kim N, Testa D, Ribot J, Morizet D, Bernard C, Jourdren L, Blugeon C, Di Nardo AA, Prochiantz A (2019) Non‐cell autonomous OTX2 homeoprotein regulates visual cortex plasticity through Gadd45b/g. Cereb Cortex 29: 2384–2395 PubMed

Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t‐test and statistical inferences of gene changes. Bioinformatics 17: 509–519 PubMed

Baroncelli L, Scali M, Sansevero G, Olimpico F, Manno I, Costa M, Sale A (2016) Experience affects critical period plasticity in the visual cortex through an epigenetic regulation of histone post‐translational modifications. J Neurosci 36: 3430–3440 PubMed PMC

Bartel DP (2018) Metazoan microRNAs. Cell 173: 20–51 PubMed PMC

Baumgart M, Groth M, Priebe S, Appelt J, Guthke R, Platzer M, Cellerino A (2012) Age‐dependent regulation of tumor‐related microRNAs in the brain of the annual fish Nothobranchius furzeri . Mech Ageing Dev 133: 226–233 PubMed

Beurdeley M, Spatazza J, Lee HHC, Sugiyama S, Bernard C, Di Nardo AA, Hensch TK, Prochiantz A (2012) Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J Neurosci 32: 9429–9437 PubMed PMC

Bhattacharyya S, Zhang X, Feferman L, Johnson D, Tortella FC, Guizzetti M, Tobacman JK (2015) Decline in arylsulfatase B and Increase in chondroitin 4‐sulfotransferase combine to increase chondroitin 4‐sulfate in traumatic brain injury. J Neurochem 134: 728–739 PubMed PMC

Boggio EM, Ehlert EM, Lupori L, Moloney EB, De Winter F, Vander Kooi CW, Baroncelli L, Mecollari V, Blits B, Fawcett JW et al (2019) Inhibition of semaphorin 3A promotes ocular dominance plasticity in the adult rat visual cortex. Mol Neurobiol 56: 5987–5997 PubMed

Braasch DA, Corey DR (2001) Locked nucleic acid (LNA): fine‐tuning the recognition of DNA and RNA. Chem Biol 8: 1–7 PubMed

Carulli D, Pizzorusso T, Kwok JCF, Putignano E, Poli A, Forostyak S, Andrews MR, Deepa SS, Glant TT, Fawcett JW (2010) Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133: 2331–2347 PubMed

Chen R, D'Alessandro M, Lee C (2013) miRNAs are required for generating a time delay critical for the circadian oscillator. Curr Biol 23: 1959–1968 PubMed PMC

Chen Y, Wang Y, Ertürk A, Kallop D, Jiang Z, Weimer RM, Kaminker J, Sheng M (2014) Activity‐induced Nr4a1 regulates spine density and distribution pattern of excitatory synapses in pyramidal neurons. Neuron 83: 431–443 PubMed

Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.‐range mass accuracies and proteome‐wide protein quantification. Nat Biotechnol 26: 1367–1372 PubMed

Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794–1805 PubMed

Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z (2009) GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48 PubMed PMC

Espinosa JS, Stryker MP (2012) Development and plasticity of the primary visual cortex. Neuron 75: 230–249 PubMed PMC

Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez‐Cymering C et al (2007) MicroRNA‐29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA 104: 15805–15810 PubMed PMC

Faini G, Aguirre A, Landi S, Lamers D, Pizzorusso T, Ratto GM, Deleuze C, Bacci A (2018) Perineuronal nets control visual input via thalamic recruitment of cortical PV interneurons. eLife 7: e41520 PubMed PMC

Fawcett JW, Oohashi T, Pizzorusso T (2019) The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function. Nat Rev Neurosci 20: 451–465 PubMed

Fenn AM, Smith KM, Lovett‐Racke AE, Guerau‐de-Arellano M, Whitacre CC, Godbout JP (2013) Increased micro‐RNA 29b in the aged brain correlates with the reduction of insulin‐like growth factor‐1 and fractalkine ligand. Neurobiol Aging 34: 2748–2758 PubMed PMC

Foscarin S, Raha‐Chowdhury R, Fawcett JW, Kwok JCF (2017) Brain ageing changes proteoglycan sulfation, rendering perineuronal nets more inhibitory. Aging 9: 1607–1622 PubMed PMC

Frenkel MY, Bear MF (2004) How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44: 917–923 PubMed

Gao M, Sossa K, Song L, Errington L, Cummings L, Hwang H, Kuhl D, Worley P, Lee HK (2010) A specific requirement of Arc/Arg3.1 for visual experience‐induced homeostatic synaptic plasticity in mouse primary visual cortex. J Neurosci 30: 7168–7178 PubMed PMC

Geaghan M, Cairns MJ (2015) MicroRNA and posttranscriptional dysregulation in psychiatry. Biol Psychiatry 78: 231–239 PubMed

Gherardini L, Gennaro M, Pizzorusso T (2015) Perilesional treatment with chondroitinase ABC and motor training promote functional recovery after stroke in rats. Cereb Cortex 25: 202–212 PubMed

Gu Y, Huang S, Chang MC, Worley P, Kirkwood A, Quinlan EM (2013) Obligatory role for the immediate early gene NARP in critical period plasticity. Neuron 79: 335–346 PubMed PMC

He M, Liu Y, Wang X, Zhang MQ, Hannon GJ, Huang ZJ (2012) Cell‐type‐based analysis of microRNA profiles in the mouse brain. Neuron 73: 35–48 PubMed PMC

Hebert SS, Horre K, Nicolai L, Papadopoulou AS, Mandemakers W, Silahtaroglu AN, Kauppinen S, Delacourte A, De Strooper B (2008) Loss of microRNA cluster miR‐29a/b‐1 in sporadic Alzheimer's disease correlates with increased BACE1/ ‐secretase expression. Proc Natl Acad Sci USA 105: 6415–6420 PubMed PMC

Heid J, Cencioni C, Ripa R, Baumgart M, Atlante S, Milano G, Scopece A, Kuenne C, Guenther S, Azzimato V et al (2017) Age‐dependent increase of oxidative stress regulates microRNA‐29 family preserving cardiac health. Sci Rep 7: 16839 PubMed PMC

Hensch TK, Quinlan EM (2018) Critical periods in amblyopia. Vis Neurosci 35: E014 PubMed PMC

Hill JJ, Jin K, Mao XO, Xie L, Greenberg DA (2012) Intracerebral chondroitinase ABC and heparan sulfate proteoglycan glypican improve outcome from chronic stroke in rats. Proc Natl Acad Sci USA 109: 9155–9160 PubMed PMC

Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98: 739–755 PubMed

Huang DW, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57 PubMed

Huang DW, Sherman BT, Lempicki RA (2009b) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1–13 PubMed PMC

Inukai S, de Lencastre A, Turner M, Slack F (2012) Novel microRNAs differentially expressed during aging in the mouse brain. PLoS ONE 7: e40028 PubMed PMC

Jassal B, Matthews L, Viteri G, Gong C, Lorente P, Fabregat A, Sidiropoulos K, Cook J, Gillespie M, Haw R et al (2019) The reactome pathway knowledgebase. Nucleic Acids Res 48: D498–D503 PubMed PMC

Jenks KR, Kim T, Pastuzyn ED, Okuno H, Taibi AV, Bito H, Bear MF, Shepherd JD (2017) Arc restores juvenile plasticity in adult mouse visual cortex. Proc Natl Acad Sci USA 114: 9182–9187 PubMed PMC

Johnson R, Zuccato C, Belyaev ND, Guest DJ, Cattaneo E, Buckley NJ (2008) A microRNA‐based gene dysregulation pathway in Huntington's disease. Neurobiol Dis 29: 438–445 PubMed

Kayala MA, Baldi P (2012) Cyber‐T web server: differential analysis of high‐throughput data. Nucleic Acids Res 40: W553–W559 PubMed PMC

Kelly EA, Russo AS, Jackson CD, Lamantia CE, Majewska AK (2015) Proteolytic regulation of synaptic plasticity in the mouse primary visual cortex: analysis of matrix metalloproteinase 9 deficient mice. Front Cell Neurosci 9: 369 PubMed PMC

Khanna S, Rink C, Ghoorkhanian R, Gnyawali S, Heigel M, Wijesinghe DS, Chalfant CE, Chan YC, Banerjee J, Huang Y et al (2013) Loss of miR‐29b following acute ischemic stroke contributes to neural cell death and infarct size. J Cereb Blood Flow Metab 33: 1197–1206 PubMed PMC

Khvorova A, Watts JK (2017) The chemical evolution of oligonucleotide therapies of clinical utility. Nat Biotechnol 35: 238–248 PubMed PMC

Kim S, Kim H, Um JW (2018) Synapse development organized by neuronal activity‐regulated immediate‐early genes. Exp Mol Med 50: 11 PubMed PMC

Klein ME, Lioy DT, Ma L, Impey S, Mandel G, Goodman RH (2007) Homeostatic regulation of MeCP2 expression by a CREB‐induced microRNA. Nat Neurosci 10: 1513–1514 PubMed

Knapska E, Kaczmarek L (2004) A gene for neuronal plasticity in the mammalian brain: Zif268/Egr‐1/NGFI‐A/Krox‐24/TIS8/ZENK? Prog Neurobiol 74: 183–211 PubMed

Kobayashi Y, Ye Z, Hensch TK (2015) Clock genes control cortical critical period timing. Neuron 86: 264–275 PubMed PMC

Kobayashi M, Benakis C, Anderson C, Moore MJ, Poon C, Uekawa K, Dyke JP, Fak JJ, Mele A, Park CY et al (2019) AGO CLIP reveals an activated network for acute regulation of brain glutamate homeostasis in ischemic stroke. Cell Rep 28: 979–991 PubMed PMC

Kole AJ, Swahari V, Hammond SM, Deshmukh M (2011) miR‐29b is activated during neuronal maturation and targets BH3‐only genes to restrict apoptosis. Genes Dev 25: 125–130 PubMed PMC

Koopmans F, van Nierop P, Andres‐Alonso M, Byrnes A, Cijsouw T, Coba MP, Cornelisse LN, Farrell RJ, Goldschmidt HL, Howrigan DP et al (2019) SynGO: an evidence‐based, expert‐curated knowledge base for the synapse. Neuron 103: 217–234 PubMed PMC

Krishnan K, Wang B‐S, Lu J, Wang L, Maffei A, Cang J, Huang ZJ (2015) MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex. Proc Natl Acad Sci USA 112: E4782–E4791 PubMed PMC

Kuc C, Richard DJ, Johnson S, Bragg L, Servos MR, Doxey AC, Craig PM (2017) Rainbow trout exposed to benzo[a]pyrene yields conserved microRNA binding sites in DNA methyltransferases across 500 million years of evolution. Sci Rep 7: 16843 PubMed PMC

Lensjø KK, Lepperød ME, Dick G, Hafting T, Fyhn M (2017) Removal of perineuronal nets unlocks juvenile plasticity through network mechanisms of decreased inhibition and increased gamma activity. J Neurosci 37: 1269–1283 PubMed PMC

Levelt CN, Hübener M (2012) Critical‐period plasticity in the visual cortex. Annu Rev Neurosci 35: 309–330 PubMed

Lippi G, Steinert JR, Marczylo EL, D'Oro S, Fiore R, Forsythe ID, Schratt G, Zoli M, Nicotera P, Young KW (2011) Targeting of the Arpc3 actin nucleation factor by miR‐29a/b regulates dendritic spine morphology. J Cell Biol 194: 889–904 PubMed PMC

Lippi G, Fernandes CC, Ewell LA, John D, Romoli B, Curia G, Taylor SR, Frady EP, Jensen AB, Liu JC et al (2016) MicroRNA‐101 regulates multiple developmental programs to constrain excitation in adult neural networks. Neuron 92: 1337–1351 PubMed PMC

Mataga N, Mizuguchi Y, Hensch TK (2004) Experience‐dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44: 1031–1041 PubMed

Mazziotti R, Baroncelli L, Ceglia N, Chelini G, Sala GD, Magnan C, Napoli D, Putignano E, Silingardi D, Tola J et al (2017a) Mir‐132/212 is required for maturation of binocular matching of orientation preference and depth perception. Nat Commun 8: 15488 PubMed PMC

Mazziotti R, Baroncelli L, Ceglia N, Chelini G, Sala GD, Magnan C, Napoli D, Putignano E, Silingardi D, Tola J et al (2017b) Gene Expression Omnibus GSE95649 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE95649) [DATASET] PubMed PMC

McCurry CL, Shepherd JD, Tropea D, Wang KH, Bear MF, Sur M (2010) Loss of Arc renders the visual cortex impervious to the effects of sensory experience or deprivation. Nat Neurosci 13: 450–457 PubMed PMC

Miyata S, Komatsu Y, Yoshimura Y, Taya C, Kitagawa H (2012) Persistent cortical plasticity by upregulation of chondroitin 6‐sulfation. Nat Neurosci 15: 414–422 PubMed

Mo J, Kim C‐H, Lee D, Sun W, Lee HW, Kim H (2015) Early growth response 1 (Egr‐1) directly regulates GABAA receptor α2, α4, and θ subunits in the hippocampus. J Neurochem 133: 489–500 PubMed

Morita S, Horii T, Kimura M, Ochiya T, Tajima S, Hatada I (2013) miR‐29 represses the activities of DNA methyltransferases and DNA demethylases. Int J Mol Sci 14: 14647–14658 PubMed PMC

Murase S, Lantz CL, Quinlan EM (2017) Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP‐9. eLife 6: e27345 PubMed PMC

Nolan K, Mitchem MR, Jimenez‐Mateos EM, Henshall DC, Concannon CG, Prehn JHM (2014) Increased expression of microRNA‐29a in ALS mice: functional analysis of its inhibition. J Mol Neurosci 53: 231–241 PubMed

Oray S, Majewska A, Sur M (2004) Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44: 1021–1030 PubMed

Ouyang Y‐B, Xu L, Lu Y, Sun X, Yue S, Xiong X‐X, Giffard RG (2013) Astrocyte‐enriched miR‐29a targets PUMA and reduces neuronal vulnerability to forebrain ischemia. Glia 61: 1784–1794 PubMed PMC

Pantazopoulos H, Woo T‐UW, Lim MP, Lange N, Berretta S (2010) Extracellular matrix‐glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch Gen Psychiatry 67: 155–166 PubMed PMC

Pantazopoulos H, Markota M, Jaquet F, Ghosh D, Wallin A, Santos A, Caterson B, Berretta S (2015) Aggrecan and chondroitin‐6‐sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala. Transl Psychiat 5: e496 PubMed PMC

Pantazopoulos H, Berretta S (2016) In sickness and in health: perineuronal nets and synaptic plasticity in psychiatric disorders. Neural Plast 2016: 9847696 PubMed PMC

Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298: 1248–1251 PubMed

Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L (2006) Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci USA 103: 8517–8522 PubMed PMC

Putignano E, Lonetti G, Cancedda L, Ratto G, Costa M, Maffei L, Pizzorusso T (2007) Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity. Neuron 54: 177 PubMed

Rajman M, Schratt G (2017) MicroRNAs in neural development: from master regulators to fine‐tuners. Development 144: 2310–2322 PubMed

Reichelt AC, Hare DJ, Bussey TJ, Saksida LM (2019) Perineuronal nets: plasticity, protection, and therapeutic potential. Trends Neurosci 42: 458–470 PubMed

Ripa R, Dolfi L, Terrigno M, Pandolfini L, Savino A, Arcucci V, Groth M, Terzibasi Tozzini E, Baumgart M, Cellerino A (2017) MicroRNA miR‐29 controls a compensatory response to limit neuronal iron accumulation during adult life and aging. BMC Biol 15: 9 PubMed PMC

Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA‐sequencing and microarray studies. Nucleic Acids Res 43: e47 PubMed PMC

Rowlands D, Lensjø KK, Dinh T, Yang S, Andrews MR, Hafting T, Fyhn M, Fawcett JW, Dick G (2018) Aggrecan directs extracellular matrix‐mediated neuronal plasticity. J Neurosci 38: 10102–10113 PubMed PMC

Rupaimoole R, Slack FJ (2017) MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat. Rev. Drug Discov. 16: 203–222 PubMed

Sato M, Stryker MP (2008) Distinctive features of adult ocular dominance plasticity. J Neurosci 28: 10278–10286 PubMed PMC

Silingardi D, Scali M, Belluomini G, Pizzorusso T (2010) Epigenetic treatments of adult rats promote recovery from visual acuity deficits induced by long‐term monocular deprivation. Eur J Neurosci 31: 2185–2192 PubMed

Silpananta P, Dunstone JR, Ogston AG (1967) Fractionation of a hyaluronic acid preparation in a density gradient. The isolation and identification of a chondroitin sulphate. Biochem J 104: 404–409 PubMed PMC

Smith CIE, Edvard Smith CI, Zain R (2019) Therapeutic oligonucleotides: state of the art. Annu Rev Pharmacol Toxicol 59: 605–630 PubMed

Soleman S, Yip PK, Duricki DA, Moon LDF (2012) Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats. Brain 135: 1210–1223 PubMed PMC

Somel M, Guo S, Fu N, Yan Z, Hu HY, Xu Y, Yuan Y, Ning Z, Hu Y, Menzel C et al (2010) MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res 20: 1207–1218 PubMed PMC

Sorg BA, Berretta S, Blacktop JM, Fawcett JW, Kitagawa H, Kwok JCF, Miquel M (2016) Casting a wide net: role of perineuronal nets in neural plasticity. J Neurosci 36: 11459–11468 PubMed PMC

Spatazza J, Lee HHC, Di Nardo AA, Tibaldi L, Joliot A, Hensch TK, Prochiantz A (2013) Choroid‐plexus‐derived Otx2 homeoprotein constrains adult cortical plasticity. Cell Rep 3: 1815–1823 PubMed PMC

Spolidoro M, Putignano E, Munafò C, Maffei L, Pizzorusso T (2012) Inhibition of matrix metalloproteinases prevents the potentiation of nondeprived‐eye responses after monocular deprivation in juvenile rats. Cereb Cortex 22: 725–734 PubMed

Steinfeld I, Navon R, Ach R, Yakhini Z (2013) miRNA target enrichment analysis reveals directly active miRNAs in health and disease. Nucleic Acids Res 41: e45 PubMed PMC

Stroud H, Su SC, Hrvatin S, Greben AW, Renthal W, Boxer LD, Nagy MA, Hochbaum DR, Kinde B, Gabel HW et al (2017) Early‐life gene expression in neurons modulates lasting epigenetic states. Cell 171: 1151–1164 PubMed PMC

Takahashi M, Eda A, Fukushima T, Hohjoh H (2012) Reduction of type IV collagen by upregulated miR‐29 in normal elderly mouse and klotho‐deficient, senescence‐model mouse. PLoS ONE 7: e48974 PubMed PMC

Takesian AE, Hensch TK (2013) Balancing plasticity/stability across brain development. Prog Brain Res 207: 3–34 PubMed

Tasic B, Menon V, Nguyen TN, Kim TK, Jarsky T, Yao Z, Levi B, Gray LT, Sorensen SA, Dolbeare T et al (2016) Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat Neurosci 19: 335–346 PubMed PMC

Tognini P, Putignano E, Coatti A, Pizzorusso T (2011) Experience‐dependent expression of miR‐132 regulates ocular dominance plasticity. Nat Neurosci 14: 1237–1239 PubMed PMC

Tognini P, Napoli D, Tola J, Silingardi D, Della Ragione F, D'Esposito M, Pizzorusso T (2015) Experience‐dependent DNA methylation regulates plasticity in the developing visual cortex. Nat Neurosci 18: 956–958 PubMed

Ugalde AP, Ramsay AJ, de la Rosa J, Varela I, Mariño G, Cadiñanos J, Lu J, Freije JM, López‐Otín C (2011) Aging and chronic DNA damage response activate a regulatory pathway involving miR‐29 and p53. EMBO J 30: 2219–2232 PubMed PMC

Vierci G, Pannunzio B, Bornia N, Rossi FM (2016) H3 and H4 lysine acetylation correlates with developmental and experimentally induced adult experience‐dependent plasticity in the mouse visual cortex. J Exp Neurosci 10: 49–64 PubMed PMC

Wen TH, Afroz S, Reinhard SM, Palacios AR, Tapia K, Binder DK, Razak KA, Ethell IM (2018a) Genetic reduction of matrix metalloproteinase‐9 promotes formation of perineuronal nets around parvalbumin‐expressing interneurons and normalizes auditory cortex responses in developing Fmr1 knock‐out mice. Cereb Cortex 28: 3951–3964 PubMed PMC

Wen TH, Binder DK, Ethell IM, Razak KA (2018b) The perineuronal ‘safety’ net? Perineuronal net abnormalities in neurological disorders. Front Mol Neurosci 11: 270 PubMed PMC

Wiersma AM, Fouad K, Winship IR (2017) Enhancing spinal plasticity amplifies the benefits of rehabilitative training and improves recovery from stroke. J Neurosci 37: 10983–10997 PubMed PMC

Yang S, Hilton S, Alves JN, Saksida LM, Bussey T, Matthews RT, Kitagawa H , Spillantini MG, Kwok JCF, Fawcett JW (2017) Antibody recognizing 4‐sulfated chondroitin sulfate proteoglycans restores memory in tauopathy‐induced neurodegeneration. Neurobiol Aging 59: 197–209 PubMed

Yoo M, Khaled M, Gibbs KM, Kim J, Kowalewski B, Dierks T, Schachner M (2013) Arylsulfatase B improves locomotor function after mouse spinal cord injury. PLoS ONE 8: e57415 PubMed PMC

Zhang X, Bhattacharyya S, Kusumo H, Goodlett CR, Tobacman JK, Guizzetti M (2014) Arylsulfatase B modulates neurite outgrowth via astrocyte chondroitin‐4‐sulfate: dysregulation by ethanol. Glia 62: 259–271 PubMed PMC

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