Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons
Open accessAbstract
Ocular dominance plasticity in the developing primary visual cortex is initiated by monocular deprivation (MD) and consolidated during subsequent sleep. To clarify how visual experience and sleep affect neuronal activity and plasticity, we continuously recorded extragranular visual cortex fast-spiking (FS) interneurons and putative principal (i.e., excitatory) neurons in freely behaving cats across periods of waking MD and post-MD sleep. Consistent with previous reports in mice, MD induces two related changes in FS interneurons: a response shift in favor of the closed eye and depression of firing. Spike-timing–dependent depression of open-eye–biased principal neuron inputs to FS interneurons may mediate these effects. During post-MD nonrapid eye movement sleep, principal neuron firing increases and becomes more phase-locked to slow wave and spindle oscillations. Ocular dominance (OD) shifts in favor of open-eye stimulation—evident only after post-MD sleep—are proportional to MD-induced changes in FS interneuron activity and to subsequent sleep-associated changes in principal neuron activity. OD shifts are greatest in principal neurons that fire 40–300 ms after neighboring FS interneurons during post-MD slow waves. Based on these data, we propose that MD-induced changes in FS interneurons play an instructive role in ocular dominance plasticity, causing disinhibition among open-eye–biased principal neurons, which drive plasticity throughout the visual cortex during subsequent sleep.
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- Authors
- Aton, S. J., Broussard, C., Dumoulin, M., Seibt, J., Watson, A., Coleman, T., & Frank, M. G.
- Affiliations
- University of Michigan (US)
- University of Pennsylvania (US)
- Departments of aNeuroscience and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-01-08
- Volume
- 110
- Issue
- 8
- Pages
- 3101-3106
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3581875
- OpenAlex
- W2059879249
- Cited by
- 113
- References
- 34
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 6 · 2023: 6 · 2022: 12 · 2021: 8 · 2020: 10 · 2019: 8 · 2018: 8 · 2017: 14 · 2016: 7 · 2015: 8 · 2014: 7 · 2013: 9
- FWCI
- 5.67
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL114161, T32HL007953)
- National Eye Institute (R01EY019022, R00EY021503, F32EY017766, K99EY021503)
- 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, monocular deprivation, fast-spiking interneurons, principal neurons, primary visual cortex, spike-timing-dependent plasticity, slow waves, sleep spindles, disinhibition, neuronal firing patterns, cats
- MeSH terms
- Action Potentials, Animals, Cats, Cerebral Cortex, Neuronal Plasticity, Neurons, Sleep, Vision, Ocular, Wakefulness
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