Experience and Activity-Dependent Maturation of Perisomatic GABAergic Innervation in Primary Visual Cortex during a Postnatal Critical Period
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The neocortical GABAergic network consists of diverse interneuron cell types that display distinct physiological properties and target their innervations to subcellular compartments of principal neurons. Inhibition directed toward the soma and proximal dendrites is crucial in regulating the output of pyramidal neurons, but the development of perisomatic innervation is poorly understood because of the lack of specific synaptic markers. In the primary visual cortex, for example, it is unknown whether, and to what extent, the formation and maturation of perisomatic synapses are intrinsic to cortical circuits or are regulated by sensory experience. Using bacterial artificial chromosome transgenic mice that label a defined class of perisomatic synapses with green fluorescent protein, here we show that perisomatic innervation developed during a protracted postnatal period after eye opening. Maturation of perisomatic innervation was significantly retarded by visual deprivation during the third, but not the fifth, postnatal week, implicating an important role for sensory input. To examine the role of cortical intrinsic mechanisms, we developed a method to visualize perisomatic synapses from single basket interneurons in cortical organotypic cultures. Characteristic perisomatic synapses formed through a stereotyped process, involving the extension of distinct terminal branches and proliferation of perisomatic boutons. Neuronal spiking in organotypic cultures was necessary for the proliferation of boutons and the extension, but not the maintenance, of terminal branches. Together, our results suggest that although the formation of perisomatic synapses is intrinsic to the cortex, visual experience can influence the maturation and pattern of perisomatic innervation during a postnatal critical period by modulating the level of neural activity within cortical circuits.
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Previous observations in sensory cortex show a reduction in inhibition after sensory deprivation.
“in line with previous observations in sensory cortex showing a reduction in inhibition after sensory deprivation”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Chattopadhyaya et al., 2004
The increase in GAD67 in MeCP2-null V1 is more prominent in PV-expressing cells.
“This increased GAD67 expression was more prominent in PV-expressing cells, most of which mature into fastspiking basket interneurons (24).”
From MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex (2015) · cites this paper as [24]
The maturation of parvalbumin interneurons is activity-dependent; calcium entry is necessary for maturation of perineuronal nets and parvalbumin interneurons, and activation of NR2A-containing NMDARs contributes to the molecular signaling that leads to maturation of these cells.
“Indeed, the maturation of PVI is activity-dependent (Chattopadhyaya et al., 2004; Patz et al., 2004). Calcium entrance is necessary for the maturation of PNN (Dityatev et al., 2007) and PVI (Jiang and Swann, 2005; Kinney et al., 2006), and activation of NR2A-containing NMDARs contributes to the molecular signaling that leads to the maturation of these cells (Kinney et al., 2006; Zhang and Sun, 201”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Chattopadhyaya et al., 2004
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- Authors
- Chattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G. W., Kuhlman, S. J., Welker, E., & Huang, Z. J.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- University of Lausanne (CH)
- Corresponding author
- Huang, Z. Josh
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2004-10-27
- Volume
- 24
- Issue
- 43
- Pages
- 9598-9611
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6730138
- OpenAlex
- W2096006516
- Cited by
- 596
- References
- 44
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 19 · 2023: 23 · 2022: 20 · 2021: 25 · 2020: 29 · 2019: 26 · 2018: 34 · 2017: 27 · 2016: 32 · 2015: 31 · 2014: 37 · 2013: 38 · 2012: 42
- FWCI
- 4.69
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Figshare (submittedVersion, cc-by)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- KiltHub Repository
- Funders
- Whitehall Foundation
- McKnight Foundation
- National Institutes of Health
- National Eye Institute (R01 EY 13564-01, R01EY013564)
- 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
- GABAergic interneurons, basket cells, primary visual cortex, visual deprivation, sensory experience, synapse maturation, dendritic inhibition
- MeSH terms
- Action Potentials, Animals, DNA Repair, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Interneurons, Isoenzymes, Mice, Transgenic, Neural Inhibition, Neuronal Plasticity, Recombinant Fusion Proteins, Sensory Deprivation, Synapses, Tetrodotoxin, Time Factors, Vision, Ocular, Visual Cortex, Presynaptic Terminals, Pyramidal Cells, Chromosomes, Artificial, Bacterial, Tissue Culture Techniques, Green Fluorescent Proteins, Mice
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