Canonical Organization of Layer 1 Neuron-Led Cortical Inhibitory and Disinhibitory Interneuronal Circuits
Open accessAbstract
Interneurons play a key role in cortical function and dysfunction, yet organization of cortical interneuronal circuitry remains poorly understood. Cortical Layer 1 (L1) contains 2 general GABAergic interneuron groups, namely single bouquet cells (SBCs) and elongated neurogliaform cells (ENGCs). SBCs predominantly make unidirectional inhibitory connections (SBC→) with L2/3 interneurons, whereas ENGCs frequently form reciprocal inhibitory and electric connections (ENGC↔) with L2/3 interneurons. Here, we describe a systematic investigation of the pyramidal neuron targets of L1 neuron-led interneuronal circuits in the rat barrel cortex with simultaneous octuple whole-cell recordings and report a simple organizational scheme of the interneuronal circuits. Both SBCs→ and ENGC ↔ L2/3 interneuronal circuits connect to L2/3 and L5, but not L6, pyramidal neurons. SBC → L2/3 interneuronal circuits primarily inhibit the entire dendritic-somato-axonal axis of a few L2/3 and L5 pyramidal neurons located within the same column. In contrast, ENGC ↔ L2/3 interneuronal circuits generally inhibit the distal apical dendrite of many L2/3 and L5 pyramidal neurons across multiple columns. Finally, L1 interneuron-led circuits target distinct subcellular compartments of L2/3 and L5 pyramidal neurons in a L2/3 interneuron type-dependent manner. These results suggest that L1 neurons form canonical interneuronal circuits to control information processes in both supra- and infragranular cortical layers.
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In rodent layer 1, high-throughput electrophysiology found two interneuron types and two canonical pathways involving feedforward interneuron-to-interneuron connections.
“Moreover, when assessing layer 1 canonical inhibitory pathways in rodent with high throughput electrophysiology capable of sampling all cell types in layer 1, Lee at al.42 found two interneuron types and two canonical pathways involving feed forward interneuron-to-interneuron connections.”
From Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type (2018) · cites this paper as [42]
Focal intralayer inhibition restricted by the compact axonal arbor of RCs to distal dendrites of a column of pyramidal cells is missing from the rodent; instead, mouse feedforward inhibitory connections are vertically spread to all somatodendritic domains.
“Furthermore, focal intralayer inhibition restricted by the compact axonal arbor of RCs to distal dendrites of a column of pyramidal cells is also missing from the rodent; rather, mouse feedforward inhibitory connections are vertically spread to all somatodendritic domains42.”
From Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type (2018) · cites this paper as [42]
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- Authors
- Lee, A. J., Wang, G., Jiang, X., Johnson, S. M., Hoang, E. T., Lanté, F., Stornetta, R. L., Beenhakker, M. P., Shen, Y., & Julius Zhu, J.
- Affiliations
- University of Virginia (US)
- Zhejiang University (CN)
- Corresponding author
- Lee, Alice J.
- ORCID
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-02-18
- Volume
- 25
- Issue
- 8
- Pages
- 2114-2126
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC4494026
- OpenAlex
- W2104708771
- Cited by
- 94
- References
- 72
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 8 · 2023: 7 · 2022: 5 · 2021: 12 · 2020: 7 · 2019: 5 · 2018: 9 · 2017: 7 · 2016: 14 · 2015: 10 · 2014: 1
- FWCI
- 4.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cerebral Cortex (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS091452)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- pyramidal neurons, GABAergic inhibition, disinhibition, barrel cortex, dendritic inhibition, subcellular targeting
- MeSH terms
- Animals, Female, Interneurons, Male, Microscopy, Electron, Neural Inhibition, Neural Pathways, Somatosensory Cortex, Synapses, Vibrissae, Rats, Sprague-Dawley, Pyramidal Cells, Patch-Clamp Techniques, Tissue Culture Techniques
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