Cited by 415Visual perception and processing mechanismsNeuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanisms

Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation

Maffei, Arianna, Nelson, Sacha B, Turrigiano, Gina G·2004·Nature Neuroscience

Abstract

Visual deprivation during a developmental sensitive period markedly alters visual cortical response properties, but the changes in intracortical circuitry that underlie these effects are poorly understood. Here we use a slice preparation of rat primary visual cortex to show that 2 d of prior visual deprivation early in life increases the excitability of layer 4 circuitry. Slice recordings showed that spontaneous activity of layer 4 star pyramidal neurons increased 25-fold after 2 d of visual deprivation between postnatal days (P) 15 and P17. This effect was mediated by increased net excitatory and decreased net inhibitory synaptic drive. Paired recordings showed that excitatory connections between star pyramidal neurons doubled in amplitude, whereas inhibitory connections decreased or increased depending on the interneuron class. These effects reversed when vision was restored. This dynamic adjustment of the excitation-inhibition balance may allow the networks within layer 4 to maintain stable levels of activity in the face of variable sensory input.

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Crossref · 10.1038/nn1351

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  • Homeostatic regulation of inhibition involves coordinated changes in postsynaptic strength, synapse number, and likely presynaptic release probability.

    “Interestingly, both in vitro and in vivo studies have documented that homeostatic regulation of inhibition involves coordinated changes in postsynaptic strength, synapse number, and likely presynaptic release probability (Kilman et al. 2002;Maffei et al. 2004;Hartman et al. 2006).”
  • Inhibitory synapses onto pyramidal neurons are regulated in the opposite direction from excitatory synapses in response to a drop in activity or sensory drive, both in vitro and in vivo.

    “Further, it has been shown both in vitro and in vivo that inhibitory synapses onto pyramidal neurons are regulated in the opposite direction from excitatory synapses in response to a drop in activity or sensory drive (Kilman et al. 2002;Vale and Sanes 2002;Maffei et al. 2004;Hartman et al. 2006;Huupponen et al. 2007).”
  • In visual cortical microcircuits, the locus of homeostatic plasticity changes as the circuit matures: early in postnatal development layer 4 responds homeostatically to brief (2 days) inactivation of the optic nerve with TTX, whereas later this response turns off in layer 4 and migrates to layers 2/3, where it persists into adulthood.

    “Interestingly, in visual cortical microcircuits the locus of homeostatic plasticity changes as the circuit matures.Early in postnatal development layer 4 (the first input layer to cortex, and the first layer to mature) responds homeostatically to brief (2 days) inactivation of the optic nerve with TTX (Desai et al. 2002;Maffei et al. 2004), whereas later (at the opening of the classical visual”
  • When sensory drive to primary visual cortex is lowered in vivo, connections from fast-spiking basket cells onto layer 4 pyramidal neurons are reduced in amplitude, whereas connections from another class of interneuron become sparser but stronger.

    “When sensory drive to primary visual cortex is lowered in vivo, connections from fast-spiking basket cells onto layer 4 pyramidal neurons are reduced in amplitude, whereas connections from another class of interneuron become sparser but stronger (Maffei et al. 2004).”
  • In neocortical networks, the net effects of changes in excitation and inhibition appear homeostatic.

    “Although in neocortical networks the net effects of changes in excitation and inhibition appear to be homeostatic (Rutherford et al. 1998;Turrigiano et al. 1998;Maffei et al. 2004), different classes of inhibitory synapse are regulated differently by lowered activity.”

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Authors
Maffei, A., Nelson, S. B., & Turrigiano, G. G.
Affiliations
Brandeis University (US)
Corresponding author
Turrigiano, Gina G
Venue
Nature Neuroscience
Published
2004-11-14
Volume
7
Issue
12
Pages
1353-1359
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
OpenAlex
W2007532471
Cited by
415
References
4
Citations by year
2026: 5 · 2025: 16 · 2024: 16 · 2023: 19 · 2022: 14 · 2021: 12 · 2020: 16 · 2019: 11 · 2018: 16 · 2017: 20 · 2016: 23 · 2015: 18 · 2014: 23 · 2013: 29 · 2012: 13
FWCI
9.90
Type
journal article
Language
en
Open access
closed
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institute on Drug Abuse (DA16455, R01DA016455)
  • National Eye Institute (EY014439, R01EY014439)
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
visual deprivation, layer 4, primary visual cortex, excitation-inhibition balance, synaptic plasticity, spontaneous activity, interneurons, vision restoration, cortical circuits
MeSH terms
Animals, Animals, Newborn, Nerve Net, Synaptic Transmission, Neuronal Plasticity, Sensory Deprivation, Visual Cortex, Vision, Monocular, Rats

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