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Critical periods in amblyopia

Published online by Cambridge University Press:  16 April 2018

TAKAO K. HENSCH  and
ELIZABETH M. QUINLAN
TAKAO K. HENSCH*
Affiliation:
FM Kirby Neurobiology Center, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts
ELIZABETH M. QUINLAN*
Affiliation:
Neuroscience and Cognitive Science Program, Department of Biology, University of Maryland, College Park, Maryland
*
*Address correspondence to: Takao K. Hensch. E-mail: hensch@mc.harvard.edu or Elizabeth M. Quinlan. E-mail: equinlan@umd.edu
*Address correspondence to: Takao K. Hensch. E-mail: hensch@mc.harvard.edu or Elizabeth M. Quinlan. E-mail: equinlan@umd.edu
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Abstract

The shift in ocular dominance (OD) of binocular neurons induced by monocular deprivation is the canonical model of synaptic plasticity confined to a postnatal critical period. Developmental constraints on this plasticity not only lend stability to the mature visual cortical circuitry but also impede the ability to recover from amblyopia beyond an early window. Advances with mouse models utilizing the power of molecular, genetic, and imaging tools are beginning to unravel the circuit, cellular, and molecular mechanisms controlling the onset and closure of the critical periods of plasticity in the primary visual cortex (V1). Emerging evidence suggests that mechanisms enabling plasticity in juveniles are not simply lost with age but rather that plasticity is actively constrained by the developmental up-regulation of molecular ‘brakes’. Lifting these brakes enhances plasticity in the adult visual cortex, and can be harnessed to promote recovery from amblyopia. The reactivation of plasticity by experimental manipulations has revised the idea that robust OD plasticity is limited to early postnatal development. Here, we discuss recent insights into the neurobiology of the initiation and termination of critical periods and how our increasingly mechanistic understanding of these processes can be leveraged toward improved clinical treatment of adult amblyopia.

Keywords

GABAParvalbuminPerineuronal netDark exposureAcetylcholinePSD-95HDAC
Type
Perspective
Information
Visual Neuroscience , Volume 35 , 2018 , E014
Copyright
Copyright © Cambridge University Press 2018 

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References

Antonini, A., Fagiolini, M. & Stryker, M.P. (1999). Anatomical correlates of functional plasticity in mouse visual cortex. Journal of Neuroscience 19, 4388–4406.CrossRefGoogle ScholarPubMed
Antonini, A. & Stryker, M.P. (1993). Rapid remodeling of axonal arbors in the visual cortex. Science 260, 1819–1821.CrossRefGoogle ScholarPubMed
Aton, S.J., Broussard, C., Dumoulin, M., Seibt, J., Watson, A., Coleman, T. & Frank, M.G. (2013). Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons. Proceedings of the National Academy of Sciences of the United States of America 110, 3101–3106.Google Scholar
Atwal, J.K., Pinkston-Gosse, J., Syken, J., Stawicki, S., Wu, Y., Shatz, C. & Tessier-Lavigne, M. (2008). PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322, 967–970.CrossRefGoogle ScholarPubMed
Baroncelli, L., Sale, A., Viegi, A., Maya Vetencourt, J.F., De Pasquale, R., Baldini, S. & Maffei, L. (2010). Experience-dependent reactivation of ocular dominance plasticity in the adult visual cortex. Experimental Neurology 226, 100–109.Google Scholar
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. Journal of Neuroscience 36, 3430–3440.Google Scholar
Bavelier, D., Levi, D.M., Li, R.W., Dan, Y. & Hensch, T.K. (2010). Removing brakes on adult brain plasticity: From molecular to behavioral interventions. Journal of Neuroscience 30, 14964–14971.Google Scholar
Beurdeley, M., Spatazza, J., Lee, H.H., Sugiyama, S., Bernard, C., Di Nardo, A.A., Hensch, T.K. & Prochiantz, A. (2012). Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. Journal of Neuroscience 32, 9429–9437.Google Scholar
Blakemore, C., Garey, L.J. & Vital-Durand, F. (1978). The physiological effects of monocular deprivation and their reversal in the monkey’s visual cortex. Journal de Physiologie 283, 223–262.Google Scholar
Bochner, D.N., Sapp, R.W., Adelson, J.D., Zhang, S., Lee, H., Djurisi, M., Syken, J., Dan, Y. & Shatz, C.J. (2014). Blocking PirB up-regulates spines and functional synapses to unlock visual cortical plasticity and facilitate recovery from amblyopia. Science Translational Medicine 6, 258ra140.Google Scholar
Bonaccorsi, J., Berardi, N. & Sale, A. (2014). Treatment of amblyopia in the adult: Insights from a new rodent model of visual perceptual learning. Frontiers in Neural Circuits 8, 82.CrossRefGoogle ScholarPubMed
Carulli, D., Pizzorusso, T., Kwok, J.C., Putignano, E., Poli, A., Forostyak, S., Andrews, M.R., Deepa, S.S., Glant, T.T. & Fawcett, J.W. (2010). Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133, 2331–2347.Google Scholar
Caspi, A., Vishne, T., Reichenberg, A., Weiser, M., Dishon, A., Lubin, G., Shmushkevitz, M., Mandel, Y., Noy, S. & Davidson, M. (2009). Refractive errors and schizophrenia. Schizophrenia Research 107, 238–241.Google Scholar
Chang, M.C., Park, J.M., Pelkey, K.A., Grabenstatter, H.L., Xu, D., Linden, D.J., Sutula, T.P., McBain, C.J. & Worley, P.F. (2010). Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons. Nature Neuroscience 13, 1090–1097.Google Scholar
Coleman, J.E., Nahmani, M., Gavornik, J.P., Haslinger, R., Heynen, A.J., Erisir, A. & Bear, M.F. (2010). Rapid structural remodeling of synapses parallels experience-dependent functional plasticity in mouse primary visual cortex. Journal of Neuroscience 30, 9670–9682.Google Scholar
Cooper, L.N. & Bear, M.F. (2012). The BCM theory of synapse modification at 30: Interaction of theory with experiment. Nature Reviews Neuroscience 13, 798–810.Google Scholar
Daw, N.W. (1998). Critical periods and amblyopia. Archives of Ophthalmology 116, 502–505.Google Scholar
Daw, N.W. (2013). Visual Development (2nd ed.). New York: Springer.Google Scholar
Daw, N.W. & Wyatt, H.J. (1976). Kittens reared in a unidirectional environment: Evidence for a critical period. Journal of Physiology 257, 155–170.Google Scholar
Di Cristo, G., Chattopadhyaya, B., Kuhlman, S.J., Fu, Y., Bélanger, M.C., Wu, C.Z., Rutishauser, U., Maffei, L. & Huang, Z.J. (2007). Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nature Neuroscience 10, 1569–1577.Google Scholar
Dickendesher, T.L., Baldwin, K.T., Mironova, Y.A., Koriyama, Y., Raiker, S.J., Askew, K.L., Wood, A., Geoffroy, C.G., Zheng, B., Liepmann, C.D., Katagiri, Y., Benowitz, L.I., Geller, H.M. & Giger, R.J. (2012). NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nature Neuroscience 15, 703–712.Google Scholar
Djurisic, M., Vidal, G.S., Mann, M., Aharon, A., Kim, T., Ferrao Santos, A., Zuo, Y., Hubener, M. & Shatz, C.J. (2013). PirB regulates a structural substrate for cortical plasticity. Proceedings of the National Academy of Sciences of the United States of America 110, 20771–20776.Google Scholar
Donato, F., Rompani, S.B. & Caroni, P. (2013). Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 504, 272–276.CrossRefGoogle ScholarPubMed
Duffy, K.R., Lingley, A.J., Holman, K.D. & Mitchell, D.E. (2016). Susceptibility to monocular deprivation following immersion in darkness either late into or beyond the critical period. Journal of Comparative Neurology 524, 2643–2653.Google Scholar
Duffy, K.R. & Livingstone, M.S. (2005). Loss of neurofilament labeling in the primary visual cortex of monocularly deprived monkeys. Cerebral Cortex 15, 1146–1154.Google Scholar
Duffy, K.R. & Mitchell, D.E. (2013). Darkness alters maturation of visual cortex and promotes fast recovery from monocular deprivation. Current Biology 23, 382–386.Google Scholar
Duffy, K.R., Murphy, K.M., Frosch, M.P. & Livingstone, M.S. (2007). Cytochrome oxidase and neurofilament reactivity in monocularly deprived human primary visual cortex. Cerebral Cortex 17, 1283–1291.Google Scholar
Durand, S., Patrizi, A., Quast, K.B., Hachigian, L., Pavlyuk, R., Saxena, A., Carninci, P., Hensch, T.K. & Fagiolini, M. (2012). NMDA receptor regulation prevents regression of visual cortical function in the absence of Mecp2. Neuron 76, 1078–1090.Google Scholar
Eaton, N.C., Sheehan, H.M. & Quinlan, E.M. (2016). Optimization of visual training for full recovery from severe amblyopia in adults. Learning & Memory 23, 99–103.Google Scholar
El-Shamayleh, Y., Kiorpes, L., Kohn, A. & Movshon, J.A. (2010). Visual motion processing by neurons in area MT of macque monkeys with experimental amblyopia. Journal of Neuroscience 30, 12198–12209.CrossRefGoogle Scholar
Fagiolini, M., Fritschy, J.M., Löw, K., Möhler, H., Rudolph, U. & Hensch, T.K. (2004). Specific GABA-A circuits for visual cortical plasticity. Science 303, 1681–1683.Google Scholar
Fagiolini, M. & Hensch, T.K. (2000). Inhibitory threshold for critical period activation in primary visual cortex. Nature 404, 183–186.Google Scholar
Fagiolini, M., Katagiri, H., Miyamoto, H., Mori, H., Grant, S.G., Mishina, M. & Hensch, T.K. (2003). Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling. Proceedings of the National Academy of Sciences of the United States of America 100, 2854–2859.Google Scholar
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. (1994). Functional postnatal development of the rat primary visual cortex and the role of visual experience: Dark rearing and monocular lid suture. Vision Research 34, 709–720.Google Scholar
Frenkel, M.Y. & Bear, M.F. (2004). How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44, 917–923.Google Scholar
Fu, Y., Kaneko, M., Tang, Y., Alvarez-Buylla, A. & Stryker, M.P. (2015). A cortical disinhibitory circuit for enhancing adult plasticity. Elife 2015, e05558.Google Scholar
Fu, Y., Tucciarone, J.M., Espinosa, J.S., Sheng, N., Daracy, D.P., Nicoll, R.A., Huang, Z.K. & Stryker, M.P. (2014). A cortical circuit for gain control by behavioral state. Cell 2014, 1139–1052.Google Scholar
Gervain, J., Vines, B.W., Chen, L.M., Seo, R.J., Hensch, T.K., Werker, J.F. & Young, A.H. (2013). Valproate reopens critical-period learning of absolute pitch. Frontiers in Systems Neuroscience 7, 102.CrossRefGoogle ScholarPubMed
Gil-Pagés, M., Stiles, R.J., Parks, C.A., Neier, S.C., Radulovic, M., Oliveros, A., Ferrer, A., Reed, B.K., Wilton, K.M. & Schrum, A.G. (2013). Slow angled-descent forepaw grasping (SLAG) could be incorporated into psy: An innate behavioral task for identification of individual experimental mice possessing functional vision. Behavioral and Brain Functions 9, 35.Google Scholar
Goel, A. & Lee, H.K. (2007). Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. Journal of Neuroscience 27, 6692–6700.Google Scholar
Gordon, J.A. & Stryker, M.P. (1996). Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. Journal of Neuroscience 16, 3274–3286.Google Scholar
Greifzu, F., Kalogeraki, E. & Löwel, S. (2016). Environmental enrichment preserved lifelong ocular dominance plasticity, but did not improve visual abilities. Neurobiology of Aging 41, 130–137.Google Scholar
Greifzu, J., Pielecka-Fortuna, F., Kalogeraki, E., Kremplar, K., Favaro, P.D., Schlüter, O.M. & Löwel, S. (2014). Environmental enrichment extends ocular dominance plasticity into adulthood and protects from stroke-induced impairments of plasticity. Proceedings of the National Academy of Sciences of the United States of America 111, 1150–1155.Google Scholar
Gu, Y., Huang, S., Chang, M.C., Worley, P., Kirkwood, A. & Quinlan, E.M. (2013). Obligatory role for the immediate early gene NARP in critical period plasticity. Neuron 79, 335–346.Google Scholar
Gu, Y., Tran, T., Murase, S., Borrell, A., Kirkwood, A. & Quinlan, E.M. (2016). Neuregulin-dependent regulation of fast-spiking interneuron excitability controls the timing of the critical period. Journal of Neuroscience 36, 10285–10295.Google Scholar
Guirado, R., Perez-Rando, M., Sanchez-Matarredona, D., Castrén, E. & Nacher, J. (2014). Chronic fluoxetine treatment alters the structure, connectivity and plasticity of cortical interneurons. International Journal of Neuropsychopharmacology 17, 1635–1646.Google Scholar
Guo, Y., Huang, S., de Pasquale, R., McGehrin, K., Lee, H.K., Zhao, K. & Kirkwood, A. (2012). Dark exposure extends the integration window for spike-timing-dependent plasticity. Journal of Neuroscience 32, 15027–15035.Google Scholar
Hanover, J.L., Huang, Z.J., Tonegawa, S. & Stryker, M.P. (1999). Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. Journal of Neuroscience 19, RC40.Google Scholar
Harauzov, A., Spolidoro, M., Dicristo, G., Pasquale, R.D., Cancedda, L., Pizzorusso, T., Viegi, A., Berardi, N. & Maffei, L. (2010). Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. Journal of Neuroscience 30, 361–371.Google Scholar
Harwerth, R.S., Smith, E.L., Duncan, G.C., Crawford, M.L. & von Noorden, G.K. (1986). Multiple sensitive periods in the development of the primate visual system. Science 232, 235–238.Google Scholar
He, H.Y., Hodos, W. & Quinlan, E.M. (2006). Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. Journal of Neuroscience 26, 2951–2955.Google Scholar
He, H.Y., Ray, B., Dennis, K. & Quinlan, E.M. (2007). Experience-dependent recovery of vision following chronic deprivation amblyopia. Nature Neuroscience 10, 1134–1136.Google Scholar
Hensch, T.K., Fagiolini, M., Mataga, N., Stryker, M.P., Baekkeskov, S. & Kash, S.F. (1998). Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504–1508.Google Scholar
Heimel, J.A., Hermans, J.M., Sommeijer, J.P., Neuro-Bsik Mouse Phenomics Consortium & Levelt, C.N. (2008). Genetic control of experience-dependent plasticity in the visual cortex. Genes, Brain and Behavior 7, 915–923.Google Scholar
Hess, R.F. & Thompson, B. (2015). Amblyopia and the binocular approach to its therapy. Vision Research 114, 4–16.Google Scholar
Hofer, S.B., Mrsic-Flogel, T.D., Bonhoeffer, T. & Hübener, M. (2009). Experience leaves a lasting structural trace in cortical circuits. Nature 457, 3137.Google Scholar
Huang, S., Gu, Y., Quinlan, E.M. & Kirkwood, A. (2010). A refractory period for rejuvenating GABAergic synaptic transmission and ocular dominance plasticity with dark exposure. Journal of Neuroscience 30, 16636–16642.Google Scholar
Huang, Z.J., Kirkwood, A., Pizzorusso, T., Porcialtti, V., Morales, B., Bear, M.F. & Maffei, L. (1999). BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 7965–7980.Google Scholar
Huang, X., Stodieck, S.K., Goetze, B., Cui, L., Wong, M.H., Wenzel, C., Hosand, L., Dong, Y., Löwel, S. & Schlüter, O.M. (2015). Progressive maturation of silent synapses governs the duration of a critical period. Proceedings of the National Academy of Sciences of the United States of America 112, E3131–E3140.Google Scholar
Hubel, D.H., Wiesel, T.N. & LeVay, S. (1977). Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society B: Biological Sciences 278, 377–409.Google Scholar
Iwai, Y., Fagiolini, M., Obata, K. & Hensch, T.K. (2003). Rapid critical period induction by tonic inhibition in visual cortex. Journal of Neuroscience 23, 6695–6702.Google Scholar
Kaneko, M., Stellwagen, D., Malenka, R.C. & Stryker, M.P. (2008). Tumor necrosis factor-alpha mediates one component of competitive, experience-dependent plasticity in developing visual cortex. Neuron 58, 673–680.Google Scholar
Kaneko, M. & Stryker, M. (2014). Sensory experience during locomotion promotes recovery of function in adult visual cortex. eLife 3, e02798.Google Scholar
Kameyama, K., Sohya, K., Ebina, T., Fukuda, A., Yanagawa, Y. & Tsumoto, T. (2010). Difference in binocularity and ocular dominance plasticity between GABAergic and excitatory cortical neurons. Journal of Neuroscience 30, 1551–1559.Google Scholar
Kaplan, E.S., Cooke, S.F., Komorowski, R.W., Chubykin, A.A., Thomazeau, A., Khibnik, L.A., Gavornik, J.P. & Bear, M.F. (2016). Contrasting roles for parvalbumin expressing inhibitory neurons in two forms of adult visual cortical plasticity. Elife 5, e11450.Google Scholar
Katagiri, H., Fagiolini, M. & Hensch, T.K. (2007). Optimization of somatic inhibition at critical period onset in mouse visual cortex. Neuron 53, 805–812.Google Scholar
Kawato, M., Lu, Z.L., Sagi, D., Sasaki, Y., Yu, C. & Watanabe, T. (2014). Perceptual learning–the past, present, and future. Vision Research 99, 1–4.Google Scholar
Kiorpes, L. (2015). Visual development in primates: Neural mechanisms and critical periods. Developmental Neurobiology 75, 1080–1090.Google Scholar
Kiorpes, L., Tang, C. & Movshon, J.A. (2006). Sensitivity to visual motion in amblyopic macaque monkeys. Visual Neuroscience 23, 247–256.Google Scholar
Krishnan, K., Wang, B.S., Lu, J., Wang, L., Maffei, A., Cang, J. & Huang, Z.J. (2015). MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America 112, E4782–E4791.Google Scholar
Kuhlman, S.J., Olivas, N.D., Tring, E., Ikrar, T., Xu, T. & Trachtenberg, J.T. (2013). A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 56, 908–923.Google Scholar
Lee, W.C., Huang, H., Feng, G., Sanes, J.R., Brown, E.N., So, P.T. & Nedivi, E. (2006). Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biology 4, e29.Google Scholar
Lehmann, K. & Löwel, S. (2008). Age-dependent ocular dominance plasticity in adult mice. PLoS One 3, e3120.CrossRefGoogle ScholarPubMed
Lennartsson, A., Arner, E., Fagiolini, M., Saxena, A., Andersson, R., Takahashi, H., Noro, Y., Sng, J., Sandelin, A., Hensch, T.K. & Carninci, P. (2015). Remodeling of retrotransposon elements during epigenetic induction of adult visual cortical plasticity by HDAC inhibitors. Epigenetics & Chromatin 8, 55.Google Scholar
Letzkus, J.J., Wolff, S.B., Meyer, E.M., Tovote, P., Courtin, J., Herry, C. & Lüthi, A. (2011). A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331.Google Scholar
LeVay, S., Stryker, M.P. & Shatz, C.J. (1978). Ocular dominance columns and their development in layer IV of the cat’s visual cortex: A quantitative study. Journal of Comparative Neurology 179, 223–244.Google Scholar
Levi, D.M. & Li, R.W. (2009). Perceptual learning as a potential treatment for amblyopia: A mini-review. Vision Research 49, 2535–2549.Google Scholar
Levi, D.M., Knill, D.C. & Bavelier, D. (2015). Stereopsis and amblyopia: A mini-review. Vision Research 114, 17–30.Google Scholar
Liao, D.S., Krahe, T.E., Prusky, G.T., Medina, A.E. & Ramoa, A.S. (2004). Recovery of cortical binocularity and orientation selectivity after the critical period for ocular dominance plasticity. Journal of Neurophysiology 92, 2113–2121.Google Scholar
Masuda, Y., Dumoulin, S.O., Nakadomari, S. & Wandell, B.A. (2008). V1 projection zone signals in human macular degeneration depend on task, not stimulus. Cerebral Cortex 18, 2483–2493.Google Scholar
Mataga, N., Mizaguchi, Y. & Hensch, T.K. (2004). Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44, 1031–1041.Google Scholar
Mataga, N., Nagai, N. & Hensch, T.K. (2002). Permissive proteolytic activity for visual cortical plasticity. Proceedings of the National Academy of Sciences of the United States of America 99, 7717–7721.Google Scholar
Maya Vetencourt, J.F., Sale, A., Viegi, A., Baroncelli, L., De Pasquale, R., O’Leary, O.F., Castrén, E. & Maffei, L. (2008). The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 18, 385–388.Google Scholar
McCurry, C.L., Shepherd, J.D., Tropea, D., Wang, K.H., Bear, M.F. & Sur, M. (2010). Loss of Arc renders the visual cortex impervious to the effects of sensory deprivation or experience. Nature Neuroscience 13, 450–457.CrossRefGoogle ScholarPubMed
McGee, A.W., Yang, Y., Fischer, Q.S., Daw, N.W. & Strittmatter, S.M. (2005). Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309, 2222–2226.Google Scholar
Mitchell, D.E. & Duffy, K.R. (2014). The case from animal studies for balanced binocular treatment strategies for human amblyopia. Ophthalmic and Physiological Optics 34, 129–145.Google Scholar
Mitchell, D.E. & MacKinnon, S. (2002). The present and potential impact of research on animal models for clinical treatment of stimulus deprivation amblyopia. Clinical and Experimental Optometry 85, 5–18.Google Scholar
Mitchell, D.E., MacNeill, K., Crowder, N.A., Holman, K. & Duffy, K.R. (2016). Recovery of visual functions in amblyopic animals following brief exposure to total darkness. Journal of Physiology 594, 149–167.Google Scholar
Miwa, J.M., Ibanez-Tallon, I., Crabtree, G.W., Sanchez, R., Sali, A., Role, L.W. & Heintz, N. (1999). Lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 23, 105–114.Google Scholar
Montey, K.L., Eaton, N.C. & Quinlan, E.M. (2013). Repetitive visual stimulation enhances recovery from severe amblyopia. Learning & Memory 20, 311–317.Google Scholar
Montey, K.L. & Quinlan, E.M. (2011). Recovery from chronic monocular deprivation following reactivation of thalamocortical plasticity by dark exposure. Nature Communications 2, 317.Google Scholar
Morishita, H. & Hensch, T.K. (2008). Critical period revisited: Impact on vision. Current Opinion in Neurobiology 18, 101–107.Google Scholar
Morishita, H., Miwa, J.M., Heintz, N. & Hensch, T.K. (2010). Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 330, 1238–1240.Google Scholar
Murphy, K.M., Roumeliotis, G., Williams, K., Beston, B.R. & Jones, D.G. (2015). Binocular visual training to promote recovery from monocular deprivation. Vision Research 114, 68–78.Google Scholar
Movshon, J.A. & Dürsteler, M.R. (1977). Effects of brief periods of unilateral eye closure on the kitten’s visual system. Journal of Neurophysiology 40, 1255–1265.Google Scholar
Nagakura, I., Van Wart, A., Petravicz, J., Tropea, D. & Sur, M. (2014). STAT1 regulates the homeostatic component of visual cortical plasticity via an AMPA receptor-mediated mechanism. Journal of Neuroscience 34, 10256–10263.Google Scholar
Niell, C.M. & Stryker, M.P. (2010). Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472–479.Google Scholar
O’Leary, T.P., Kutcher, M.R., Mitchell, D.E. & Duffy, K.R. (2012). Recovery of neurofilament following early monocular deprivation. Frontiers in Systems Neuroscience 6, 22.Google Scholar
Olson, C.R. & Freeman, R.D. (1975). Progressive changes in kitten striate cortex during monocular vision. Journal of Neurophysiology 38, 26–32.Google Scholar
Oray, S., Majewska, A. & Sur, M. (2004). Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44, 1021–1030.Google Scholar
Pelkey, K.A., Barksdale, E., Craig, M.T., Yuan, X., Sukumaran, M., Vargish, G.A., Mitchell, R.M., Wyeth, M.S., Petralia, R.S., Chittajallu, R., Karlsson, R.M., Cameron, H.A., Murata, Y., Colonnese, M.T., Worley, P.F. & McBain, C.J. (2015). Pentraxins coordinate excitatory synapse maturation and circuit integration of parvalbumin interneurons. Neuron 85, 1257–1272.Google Scholar
Penzes, P., Buonanno, A., Passafaro, M., Sala, C. & Sweet, R.A. (2013). Developmental vulnerability of synapses and circuits associated with neuropsychiatric disorders. Journal of Neurochemistry 126, 165–182.Google Scholar
Pfeffer, C., Xue, M., He, M., Huang, Z. & Scanziani, M. (2013). Inhibition of inhibition in visual cortex: The logic of connections between molecularly distinct interneurons. Nature Neuroscience 16, 1068–1076.Google Scholar
Pi, H.J., Hangya, B., Kvitsiani, D., Sanders, J.I., Huang, Z.J. & Kepecs, A. (2013). Cortical interneurons that specialize in disinhibitory control. Nature 503, 521–524.Google Scholar
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J.W. & Maffei, L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248–1251.Google Scholar
Pizzorusso, T., Medini, P., Landi, S., Baldini, S., Berardi, N. & Maffei, L. (2006). Structural and functional recovery from early monocular deprivation in adult rats. Proceedings of the National Academy of Sciences of the United States of America 103, 8517–8522.Google Scholar
Prusky, G.T. & Douglas, R.M. (2003). Developmental plasticity of mouse visual acuity. European Journal of Neuroscience 17, 167–173.Google Scholar
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 53, 747–759.Google Scholar
Quinlan, E.M., Philpot, B.D., Huganir, R.L. & Bear, M.F. (1999). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nature Neuroscience 2, 352–357.Google Scholar
Rico, B. & Marín, O. (2011). Neuregulin signaling, cortical circuitry development and schizophrenia. Current Opinion in Genetics & Development 21, 262–270.Google Scholar
Saiepour, M.H., Rajendran, R., Omrani, A., Ma, W.P., Tao, H.W., Heimel, J.A. & Levelt, C.N. (2015). Ocular dominance plasticity disrupts binocular inhibition-excitation matching in visual cortex. Current Biology 25, 713–721.Google Scholar
Sajo, M., Ellis-Davies, G. & Morishita, H. (2016). Lynx1 limits dendritic spine turnover in the adult visual cortex. Journal of Neuroscience 36, 9472–9478.Google Scholar
Sale, A., Maya Vetencourt, J.F., Medini, P., Cenni, M.C., Baroncelli, L., De Pasquale, R. & Maffei, L. (2007). Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nature Neuroscience 10, 679–681.Google Scholar
Sato, M. & Stryker, M.P. (2008). Distinctive features of adult ocular dominance plasticity. Journal of Neuroscience 28, 10278–10286.Google Scholar
Sawtell, N.B., Frenkel, M.Y., Philpot, B.D., Nakazawa, K., Tonegawa, S. & Bear, M.F. (2003). NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38, 977–985.Google Scholar
Scali, M., Baroncelli, L., Cenni, M.C., Sale, A. & Maffei, L. (2012). A rich environmental experience reactivates visual cortex plasticity in aged rats. Experimental Gerontology 47, 337–341.Google Scholar
Scholl, B., Burge, J. & Priebe, N.L. (2013). Binocular integration and disparity selectivity in mouse primary visual cortex. Journal of Neurophysiology 109, 3013–3024.Google Scholar
Schwarzkopf, D.S., Vorobyov, V., Mitchell, D.E. & Sengpiel, F. (2007). Brief daily binocular vision prevents monocular deprivation effects in visual cortex. European Journal of Neuroscience 25, 270–280.Google Scholar
Sengpiel, F. (2014). Plasticity of the visual cortex and treatment of amblyopia. Current Biology 24, R936–R940.Google Scholar
Shatz, C.J. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat’s visual cortex and the effects of monocular deprivation. Journal of Physiology 281, 267–283.Google Scholar
Shooner, C., Hallum, L.E., Kumbhani, R.D., Ziemba, C.M., Garcia-Marin, V., Kelly, J.G., Majaj, N.J., Movshon, J.A. & Kiorpes, L. (2015). Population representation of visual information in areas V1 and V2 of amblyopic macaques. Vision Research 114, 56–67.Google Scholar
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. European Journal of Neuroscience 31, 2185–2192.Google Scholar
Simons, K. (2005). Amblyopia characterization, treatment, and prophylaxis. Survey of Ophthalmology 50, 123–166.Google Scholar
Spatazza, J., Lee, H.H., Di Nardo, A.A., Tibaldi, L., Joliot, A., Hensch, T.K. & Prochiantz, A. (2013). Choroid-plexus-derived Otx2 homeoprotein constrains adult cortical plasticity. Cell Reports 3, 1815–1823.Google Scholar
Stephany, C.É., Chan, L.L., Parivash, S.N., Dorton, H.M., Piechowicz, M., Qiu, S. & McGee, A.W. (2014). Plasticity of binocularity and visual acuity are differentially limited by nogo receptor. Journal of Neuroscience 34, 11631–11640.Google Scholar
Stodieck, S.K., Greifzu, F., Goetze, B., Schmidt, K.F. & Löwel, S. (2014). Brief dark exposure restored ocular dominance plasticity in aging mice and after a cortical stroke. Experimental Gerontology 60, 1–11.Google Scholar
Sugiyama, S., Di Nardo, A.A., Aizawa, S., Matsuo, I., Volovitch, M., Prochiantz, A. & Hensch, T.K. (2008). Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 134, 508–520.Google Scholar
Sun, Y., Ikrar, T., Davis, M.F., Gong, N., Zheng, Z., Luo, Z.D., Lai, C., Mei, L., Holmes, T.C., Gandhi, S.P. & Xu, X. (2016). Neurogulin-1/ErbB4 signaling regulates visual cortical plasticity. Neuron 92, 160–173.Google Scholar
Syken, J., Grandpre, T., Kanold, P.O. & Shatz, C.J. (2006). PirB restricts ocular-dominance plasticity in visual cortex. Science 313, 1795–1800.Google Scholar
Taha, S. & Stryker, M.P. (2002). Rapid ocular dominance plasticity requires cortical but not geniculate protein synthesis. Neuron 34, 425–436.Google Scholar
Takesian, A.E. & Hensch, T.K. (2013). Balancing plasticity/stability across brain development. Progress in Brain Research 207, 3–34.Google Scholar
Ting, A.K., Chen, Y., Wen, L., Yin, D.M., Shen, C., Tao, Y., Liu, X., Xiong, W.C. & Mei, L. (2011). Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons. Journal of Neuroscience 31, 15–25.Google Scholar
Toyoizumi, T., Miyamoto, H., Yazaki-Sugiyama, Y., Atapour, N., Hensch, T.K. & Miller, K.D. (2013). A theory of the transition to critical period plasticity: Inhibition selectively suppresses spontaneous activity. Neuron 80, 51–63.Google Scholar
Trachtenberg, J.T. & Stryker, M.P. (2001). Rapid anatomical plasticity of horizontal connections in the developing visual cortex. Journal of Neuroscience 21, 3476–3482.Google Scholar
Trachtenberg, J.T., Trepel, C. & Stryker, M.P. (2000). Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287, 2029–2032.Google Scholar
Tropea, D., Majewska, A.K., Garcia, R. & Sur, M. (2010). Structural dynamics of synapses in vivo correlate with functional changes during experience-dependent plasticity in visual cortex. Journal of Neuroscience 30, 11086–11095.Google Scholar
Tsirlin, I., Colpa, L., Goltz, H.C. & Wong, A.M. (2015). Behavioral training as new treatment for adult amblyopia: A meta-analysis and systemic review. Investigative Ophthalmology & Visual Science 56, 4061–4075.Google Scholar
van Versendaal, D. & Levelt, C.N. (2016). Inhibitory interneurons in visual cortical plasticity. Cellular and Molecular Life Sciences 73, 3677–3691.Google Scholar
Wang, B.S., Sarnaik, R. & Cang, J. (2010). Critical period plasticity matches binocular orientation preference in the visual cortex. Neuron 65, 246–256.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology 26, 1003–1017.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal de Physiologie 206, 419–436.Google Scholar
Yang, E.J., Lin, E.W. & Hensch, T.K. (2012). Critical period for acoustic preference in mice. Proceedings of the National Academy of Sciences of the United States of America 109, 17213–17220.Google Scholar
Yashiro, K., Corlew, R. & Philpot, B.D. (2005). Visual deprivation modifies both presynaptic glutamate release and the composition of perisynaptic/extrasynaptic NMDA receptors in adult visual cortex. Journal of Neuroscience 25, 11684–11692.Google Scholar
Yazaki-Sugiyama, Y., Kang, S., Cåteau, H., Fukai, T. & Hensch, T.K. (2009). Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 462, 218–221.Google Scholar
Yu, H., Majewska, A.K. & Sur, M. (2011). Rapid experience-dependent plasticity of synapse function and structure in ferret visual cortex in vivo. Proceedings of the National Academy of Sciences of the United States of America 108, 21235–21240.Google Scholar