A Theory of the Transition to Critical Period Plasticity: Inhibition Selectively Suppresses Spontaneous Activity
Open accessAbstract
What causes critical periods (CPs) to open? For the best-studied case, ocular dominance plasticity in primary visual cortex in response to monocular deprivation (MD), the maturation of inhibition is necessary and sufficient. How does inhibition open the CP? We present a theory: the transition from pre-CP to CP plasticity arises because inhibition preferentially suppresses responses to spontaneous relative to visually driven input activity, switching learning cues from internal to external sources. This differs from previous proposals in (1) arguing that the CP can open without changes in plasticity mechanisms when activity patterns become more sensitive to sensory experience through circuit development, and (2) explaining not simply a transition from no plasticity to plasticity, but a change in outcome of MD-induced plasticity from pre-CP to CP. More broadly, hierarchical organization of sensory-motor pathways may develop through a cascade of CPs induced as circuit maturation progresses from "lower" to "higher" cortical areas.
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Different studies have found increased cortical plasticity after induction of a decrease in inhibitory activity, in some cases involving depletion of PNNs.
“Supporting this idea, different studies have found an increased cortical plasticity after the induction of a decrease in inhibitory activity, in some cases involving the depletion of PNNs (Harauzov et al., 2010;Toyoizumi et al., 2013;Lensjø et al., 2017b).”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Toyoizumi et al., 2013
The Discussion (Experimental Tests; page unavailable) lists perineuronal-net removal among paradigms that reactivate adult critical-period plasticity. But the paper does not report finding increased plasticity after experimentally decreasing inhibitory activity; for the developmental critical period it studies, the Introduction instead says that maturation or enhancement of inhibition initiates plasticity. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe desynchronization of spontaneous network activity coincides temporally with the increasing influence of sensory experience, through which external signals begin to shape synaptic connectivity by outcompeting internally generated activity.
“The desynchronization of spontaneous network activity coincides temporally with the increasing influence of sensory experience, through which external signals begin to shape synaptic connectivity by outcompeting internally generated activity 33 .”
From Developmental timing and critical windows for the treatment of psychiatric disorders (2016) · cites this paper as [33]
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References 126 · Cited by 158
Research works printed but not linked: 5
- Dayan P Abbott LF Theoretical neuroscience computational and mathematical modeling of neural systems 2001 Massachusetts Institute of Technology Press Cambridge, Mass.
- Gerstner W Kistler WM Spiking neuron models: single neurons, populations, plasticity 2002 Cambridge University Press Cambridge, U.K.; New York
- Hebb DO The organization of behavior 1949 Wiley & Sons New York
- Lenneberg EH Biological Foundations of Language 1967 Wiley New York
- Oja E Neural networks, principal components, and subspaces International journal of neural systems 1989 1 61 68
- Authors
- Toyoizumi, T., Miyamoto, H., Yazaki-Sugiyama, Y., Atapour, N., Hensch, T. K., & Miller, K. D.
- Affiliations
- Tokyo Institute of Technology (JP)
- RIKEN Center for Brain Science (JP)
- Harvard University (US)
- Columbia University (US)
- Corresponding author
- Toyoizumi, Taro
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2013-10
- Volume
- 80
- Issue
- 1
- Pages
- 51-63
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3800182
- OpenAlex
- W2100617174
- Cited by
- 158
- References
- 126
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 13 · 2023: 9 · 2022: 15 · 2021: 14 · 2020: 16 · 2019: 8 · 2018: 9 · 2017: 9 · 2016: 14 · 2015: 15 · 2014: 11 · 2013: 1
- FWCI
- 7.36
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Stryker
- National Eye Institute (R01EY011001)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- critical period, ocular dominance plasticity, monocular deprivation, inhibitory interneurons, spontaneous activity, primary visual cortex, cortical development
- MeSH terms
- Animals, Critical Period, Psychological, Learning, Neural Inhibition, Neuronal Plasticity, Photic Stimulation, Sensory Deprivation, Visual Cortex, Visual Pathways, Vision, Binocular, Vision, Monocular, Dominance, Ocular, Mice
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