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A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex
Open accessAbstract
Early sensory experience instructs the maturation of neural circuitry in the cortex. This has been studied extensively in the primary visual cortex, in which loss of vision to one eye permanently degrades cortical responsiveness to that eye, a phenomenon known as ocular dominance plasticity (ODP). Cortical inhibition mediates this process, but the precise role of specific classes of inhibitory neurons in ODP is controversial. Here we report that evoked firing rates of binocular excitatory neurons in the primary visual cortex immediately drop by half when vision is restricted to one eye, but gradually return to normal over the following twenty-four hours, despite the fact that vision remains restricted to one eye. This restoration of binocular-like excitatory firing rates after monocular deprivation results from a rapid, although transient, reduction in the firing rates of fast-spiking, parvalbumin-positive (PV) interneurons, which in turn can be attributed to a decrease in local excitatory circuit input onto PV interneurons. This reduction in PV-cell-evoked responses after monocular lid suture is restricted to the critical period for ODP and appears to be necessary for subsequent shifts in excitatory ODP. Pharmacologically enhancing inhibition at the time of sight deprivation blocks ODP and, conversely, pharmacogenetic reduction of PV cell firing rates can extend the critical period for ODP. These findings define the microcircuit changes initiating competitive plasticity during critical periods of cortical development. Moreover, they show that the restoration of evoked firing rates of layer 2/3 pyramidal neurons by PV-specific disinhibition is a key step in the progression of ODP.
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“Sensory manipulations or drug treatments that inhibit PV cells may result in PV-mediated cortical disinhibition that creates a permissive state for ODP to occur in the presence of visual experience (Kuhlman et al., 2013;Gu et al., 2016;Sun et al., 2016;Grieco et al., 2020;Sadahiro et al., 2020).”
From Psychedelics and Neural Plasticity: Therapeutic Implications (2022) · cites this paper as Kuhlman et al., 2013
In the citing paper
“First, intact PNNs may structurally limit the robust synaptic plasticity directly upon PV-cells (48–50).”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [49]
In the citing paper
“Reduction in the inhibitory output of FS basket cells has been shown to reactivate plasticity in the adult visual cortex (Kuhlman et al., 2013; Kaplan et al., 2016).”
From Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9 (2017) · cites this paper as Kuhlman et al., 2013
In the citing paper
“These networks are associated with plasticity from early life throughout adulthood [70][71][72][73].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [72]
In the citing paper
“However, this potential remains in mature circuits, as sensitivity to MD can be reestablished in adult mice by suppressing GABA synthesis or reducing PVBC firing rates (465, 614).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [614]
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Metadata
- Authors
- Kuhlman, S. J., Olivas, N. D., Tring, E., Ikrar, T., Xu, X., & Trachtenberg, J. T.
- Affiliations
- University of California, Los Angeles (US)
- University of California, Irvine (US)
- Corresponding author
- Xu, Xiangmin
- Trachtenberg, Joshua T.
- Venue
- Nature
- Published
- 2013-08-25
- Volume
- 501
- Issue
- 7468
- Pages
- 543-546
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3962838
- OpenAlex
- W2065582606
- Cited by
- 412
- References
- 47
- Citations by year
- 2026: 12 · 2025: 28 · 2024: 19 · 2023: 31 · 2022: 25 · 2021: 38 · 2020: 44 · 2019: 38 · 2018: 35 · 2017: 42 · 2016: 31 · 2015: 33 · 2014: 30 · 2013: 6
- FWCI
- 17.95
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute on Drug Abuse (R00DA023700)
- National Eye Institute (EY016052, R01EY016052, R01EY023871)
- National Institute of Neurological Disorders and Stroke (R01NS078434, NS078434)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- ocular dominance plasticity, parvalbumin interneurons, critical period, primary visual cortex, monocular deprivation, cortical inhibition, disinhibition, fast-spiking interneurons, sensory deprivation, inhibitory interneurons, eye development
- MeSH terms
- Animals, Critical Period, Psychological, Female, Interneurons, Lasers, Male, Neural Inhibition, Neuronal Plasticity, Parvalbumins, Photic Stimulation, Sensory Deprivation, Visual Cortex, Vision, Binocular, Vision, Monocular, Dominance, Ocular, Mice
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