Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator
Open accessAbstract
Sensory experience physically rewires the brain in early postnatal life through unknown processes. Here, we identify a robust anatomical consequence of monocular deprivation (MD) in layer II/III of visual cortex that corresponds to the rapid, functional loss of responsiveness preceding any changes in axonal input. Protrusions on pyramidal cell apical dendrites increased steadily after eye opening, but were transiently lost through competitive mechanisms after brief MD only during the physiological critical period. Proteolysis by tissue-type plasminogen activator (tPA) conversely declined with age and increased with MD only in young mice. Targeted disruption of tPA release or its upstream regulation by glutamic acid decarboxylase (GAD65) prevented MD-induced spine loss that was pharmacologically rescued concomitant with critical period plasticity. An extracellular mechanism for structural remodeling that is limited to the binocular zone upon proper detection of competing inputs thus links early sensory experience to visual function.
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During the critical period, monocular deprivation induces a significant decrease in the density of dendritic spines on pyramidal neurons in deprived V1b, but this plasticity is lost with age.
“During the critical period for ocular dominance plasticity, MD induces a significant decrease in the density of dendritic spines on pyramidal neurons in deprived V1b (contralateral to the occlusion), but this plasticity is lost with age (Mataga et al., 2004).”
From Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9 (2017) · cites this paper as Mataga et al., 2004
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Reh, R. K., Dias, B. G., Nelson, C. A., Kaufer, D., Werker, J. F., Kolb, B., Levine, J. D., & Hensch, T. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820836117 · Cited by 492 · see citing works
Self-citationMicroglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex
Sipe, G. O., Lowery, Tremblay, M.-È., Kelly, E. A., Lamantia, C. E., & Majewska, A. K. (2016) · Nature Communications · doi:10.1038/ncomms10905 · Cited by 512 · see citing works
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Self-citationMatrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory
Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J., Costa, R. M., Silva, A. J., Kaczmarek, L., & Huntley, G. W. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4359-05.2006 · Cited by 499 · see citing works
Critical-Period Plasticity in the Visual Cortex
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Otx2 Binding to Perineuronal Nets Persistently Regulates Plasticity in the Mature Visual Cortex
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Self-citationStructural and functional recovery from early monocular deprivation in adult rats
Pizzorusso, T., Medini, P., Landi, S., Baldini, S., Berardi, N., & Maffei, L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602657103 · Cited by 367 · see citing works
Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex
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Reducing Intracortical Inhibition in the Adult Visual Cortex Promotes Ocular Dominance Plasticity
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Critical period revisited: impact on vision
Morishita, H., & Hensch, T. K. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.05.009 · Cited by 311 · see citing works
Self-citationAutism: A “Critical Period” Disorder?
LeBlanc, J. J., & Fagiolini, M. (2011) · Neural Plasticity · doi:10.1155/2011/921680 · Cited by 301 · see citing works
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Dendritic spines: from structure to in vivo function
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Dendritic Spine Dynamics Are Regulated by Monocular Deprivation and Extracellular Matrix Degradation
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A critical period for auditory thalamocortical connectivity
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Perineuronal Nets Enhance the Excitability of Fast-Spiking Neurons
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GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling
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Rapid axonal sprouting and pruning accompany functional reorganization in primary visual cortex
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A role for microglia in synaptic plasticity?
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Converting juvenile into adult plasticity: a role for the brain's extracellular matrix
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Plasticity in the adult brain: lessons from the visual system
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Perineuronal nets and schizophrenia: The importance of neuronal coatings
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From brain formation to plasticity: Insights on Otx2 homeoprotein
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Plasticity of the visual cortex and treatment of amblyopia
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Regional and temporal specificity of intrinsic plasticity mechanisms in rodent primary visual cortex
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- Authors
- Mataga, N., Mizuguchi, Y., & Hensch, T. K.
- Affiliations
- RIKEN Center for Brain Science (JP)
- Corresponding author
- Hensch, Takao K.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2004-12
- Volume
- 44
- Issue
- 6
- Pages
- 1031-1041
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2030192664
- Cited by
- 371
- References
- 92
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 5 · 2023: 9 · 2022: 8 · 2021: 12 · 2020: 25 · 2019: 10 · 2018: 10 · 2017: 17 · 2016: 18 · 2015: 13 · 2014: 20 · 2013: 29 · 2012: 20
- FWCI
- 6.80
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 3150 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- RIKEN Brain Science Institute
- Ministry of Education, Culture, Sports, Science and Technology
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- monocular deprivation, visual cortex, critical period plasticity, tissue plasminogen activator, glutamic acid decarboxylase, layer II/III pyramidal neurons, extracellular proteolysis
- MeSH terms
- Animals, Glutamate Decarboxylase, Humans, Isoenzymes, Tissue Plasminogen Activator, Sensory Deprivation, Visual Cortex, Vision, Monocular, Mice, Knockout, Dendritic Spines, Mice
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