Complementary networks of cortical somatostatin interneurons enforce layer specific control
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Abstract
The neocortex is functionally organized into layers. Layer four receives the densest bottom up sensory inputs, while layers 2/3 and 5 receive top down inputs that may convey predictive information. A subset of cortical somatostatin (SST) neurons, the Martinotti cells, gate top down input by inhibiting the apical dendrites of pyramidal cells in layers 2/3 and 5, but it is unknown whether an analogous inhibitory mechanism controls activity in layer 4. Using high precision circuit mapping, in vivo optogenetic perturbations, and single cell transcriptional profiling, we reveal complementary circuits in the mouse barrel cortex involving genetically distinct SST subtypes that specifically and reciprocally interconnect with excitatory cells in different layers: Martinotti cells connect with layers 2/3 and 5, whereas non-Martinotti cells connect with layer 4. By enforcing layer-specific inhibition, these parallel SST subnetworks could independently regulate the balance between bottom up and top down input.
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In the Sst subclass, morpho-electric properties varied continuously across the transcriptomic landscape, with neighbouring t-types consistently showing similar morphologies and similar rebound values.
“We observed the same in the Sst subclass, which is known to be transcriptomically4 and morpho-electrically29,30,33 diverse in L5. Here we also found that morpho-electric properties varied continuously across the transcriptomic landscape, with neighbouring t-types consistently showing similar morphologies and similar rebound values (Fig. 4b).”
From Phenotypic variation of transcriptomic cell types in mouse motor cortex (2021) · cites this paper as [33]
A dominant layer 4 projection appears to be a common feature of Sst Hpse Cbln4-type neurons across cortical areas.
“A dominant L4 projection appears to be a common feature of Sst Hpse Cbln4-type neurons across cortical areas (Naka et al., 2019), while the L1 projection is not always present.”
From Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells (2020) · cites this paper as Naka et al., 2019
Recent evidence suggests that different morphological phenotypes correspond to different synaptic connectivity profiles.
“Recent evidence also suggests that different morphological phenotypes correspond to differential synaptic connectivity profiles (Nigro et al., 2018; Naka et al., 2019; Scala et al., 2019).”
From Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells (2020) · cites this paper as Naka et al., 2019
Sst Calb2 Pdlim is a Martinotti cell type and Sst Hpse Cbln4 is a non-Martinotti cell type.
“This suggests that Sst Calb2 Pdlim is a MC type, in agreement with the conclusions of Tasic et al.25 based on the data from Paul et al.46, and that Sst Hpse Cbln4 is a NMC type, in agreement with Naka et al.47.”
From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [47]
All non-fast-spiking SOM+ cells in V1 L5 and the majority of SOM+ cells in S1 L5 are known to be Martinotti cells.
“Morphologically, all non-fast-spiking SOM+ cells in V1 L529,47 and the majority of SOM+ cells in S1 L522,29,42,47 are known to be MCs.”
From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [47]
Naka et al. showed that L4 excitatory neurons connect to NMCs in L5 but not to MCs in L5.
“Within S1, Naka et al.47 showed that L4 excitatory neurons connect to NMCs in L5 but not to MCs in L5”
From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [47]
In S1 L5, L5 pyramidal cells are preferentially innervated by L5 MCs, not L5 NMCs.
“in S1 L5, where the principal excitatory cells are pyramidal and SOM+ interneurons are either L5 MC or L5 NMC, L5 pyramidal cells are preferentially innervated by L5 MCs, not L5 NMCs47.”
From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [47]
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References 116 · Cited by 117
- Authors
- Naka, A., Veit, J., Shababo, B., Chance, R. K., Risso, D., Stafford, D., Snyder, B., Egladyous, A., Chu, D., Sridharan, S., Mossing, D. P., Paninski, L., Ngai, J., & Adesnik, H.
- Affiliations
- University of California, Berkeley (US)
- University of Padua (IT)
- Columbia University (US)
- Corresponding author
- Adesnik, Hillel
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2019-03-18
- Volume
- 8
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6422636
- OpenAlex
- W2949480020
- Cited by
- 117
- References
- 116
- Citations by year
- 2026: 8 · 2025: 20 · 2024: 18 · 2023: 11 · 2022: 21 · 2021: 15 · 2020: 14 · 2019: 9
- FWCI
- 7.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Padua Research Archive (University of Padova) (submittedVersion, cc-by)
- Funders
- National Institute of Neurological Disorders and Stroke (F31NS093925, DP2NS087725-01)
- Fannie and John Hertz Foundation (Fellowship)
- National Science Foundation (Graduate Research Fellowship)
- Intelligence Advanced Research Projects Activity (D16PC00003)
- Defense Advanced Research Projects Agency (N66001-15-C-4032)
- National Institute of Mental Health (U19MH114830)
- New York Stem Cell Foundation
- 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
- somatostatin interneurons, Martinotti cells, cortical layers, barrel cortex, top-down inhibition, layer 2/3, layer 5, pyramidal neurons, inhibitory circuits, optogenetic perturbation, single-cell transcriptomics, circuit mapping, mice
- MeSH terms
- Animals, Interneurons, Nerve Net, Somatostatin, Pyramidal Cells, Neocortex, Gene Expression Profiling, Mice, Optogenetics
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