Cited by 172Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionConnexins and lens biology

Synaptic interactions of late-spiking neocortical neurons in layer 1

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Chu, Zhiguo, Galarreta, Mario, Hestrin, Shaul·2003·The Journal of Neuroscience

Abstract

Layer 1 of the neocortex is an important zone in which synaptic integration of inputs originating from a variety of cerebral regions is thought to take place. Layer 1 does not contain pyramidal cells, and several histochemical studies have suggested that most layer 1 neurons are GABAergic. However, although layer 1 neurons could be an important source of inhibition in this layer, the synaptic action of these neurons and the identity of their postsynaptic targets are unknown. We studied the physiological properties and synaptic interactions of a class of cells within layer 1 called late-spiking (LS) cells. The dendrites and axons of layer 1 LS cells were confined primarily to layer 1. Using paired recording, we showed that LS cells formed GABAergic connections with other LS cells as well as with non-LS cells in layer 1 and with pyramidal cells in layer 2/3. We also found that layer 2/3 pyramidal neurons provide excitatory inputs to LS cells. It has been suggested previously that GABAergic neurons belonging to the same class in the cortex are electrically coupled. In agreement with that hypothesis, we found that LS cells were interconnected by electrical coupling (83%), whereas electrical coupling between LS cells and non-LS cells was infrequent (2%). Thus, we provide evidence showing that a group of GABAergic neurons within layer 1 are specifically interconnected by electrical coupling and can provide significant inhibitory inputs to neurons in layer 1 and to distal dendrites of pyramidal cells.

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Crossref · 10.1523/jneurosci.23-01-00096.2003

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  • Layer 1 cells are almost all inhibitory and interconnect strongly via electrical connections and chemical synapses.

    “These L1 cells are almost all inhibitory and interconnect strongly with each other, via electrical connections and chemical synapses (Chu et al., 2003).”

    From Canonical Microcircuits for Predictive Coding (2012) · cites this paper as Chu et al., 2003

    The Abstract says histochemical studies suggest most layer 1 neurons are GABAergic, but it does not establish that almost all are inhibitory. The ‘Electrical coupling and inhibitory connections among LS cells’ section reports electrical coupling in 83% and chemical connections in 26.2% of tested late-spiking cell pairs. Those findings support interconnection within that cell class, not a strong interconnection among layer 1 cells generally. (LLM, conf=0.88)

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  • Layer 1 cells provide strong monosynaptic inhibition to L2/3 pyramidal cells whose apical dendrites project into L1.

    “Simultaneous whole cell patch clamp recordings show that they provide strong monosynaptic inhibition to L2/3 pyramidal cells, whose apical dendrites project into L1 (Chu et al., 2003; Wozny and Williams, 2011).”

    From Canonical Microcircuits for Predictive Coding (2012) · cites this paper as Chu et al., 2003

  • NGFCs of layer 2/3 (but not layer 1) of rat somatosensory cortex are highly interconnected via electrical synapses and also make widespread electrical synapses with PVBCs, regular spiking nonpyramidal cells, AACs as well as many other unidentified interneuron cell types.

    “One interesting deviation from this canonical rule are NGFCs of layer 2/3 (but not layer 1) (206) of rat somatosensory cortex. Although these cells were highly interconnected via electrical synapses, they also made widespread electrical synapses with PVBCs, regular spiking nonpyramidal cells, AACs as well as many other unidentified interneuron cell types (1017).”

    From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [206]

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Authors
Chu, Z., Galarreta, M., & Hestrin, S.
Affiliations
Stanford Medicine (US)
Venue
The Journal of Neuroscience
Published
2003-01-01
Volume
23
Issue
1
Pages
96-102
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2171308715
Cited by
172
References
38
Citations by year
2026: 3 · 2025: 3 · 2024: 4 · 2023: 2 · 2022: 5 · 2021: 1 · 2020: 8 · 2019: 4 · 2018: 11 · 2017: 6 · 2016: 10 · 2015: 8 · 2014: 10 · 2013: 6 · 2012: 16
FWCI
3.81
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • National Eye Institute (R01EY012114, EY12114, EY09120, R01EY009120)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
Keywords
GABAergic interneurons, electrical coupling, synaptic integration, pyramidal neurons, layer 2/3, inhibitory interneurons, postsynaptic targets, paired recordings
MeSH terms
Animals, Cells, Cultured, Electric Conductivity, gamma-Aminobutyric Acid, Kinetics, Neural Inhibition, Neural Pathways, Synaptic Transmission, Neurons, Rats, Sprague-Dawley, Pyramidal Cells, Patch-Clamp Techniques, Neocortex, Excitatory Postsynaptic Potentials, Rats

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