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Four Unique Interneuron Populations Reside in Neocortical Layer 1
Open accessAbstract
Sensory perception depends on neocortical computations that contextually adjust sensory signals in different internal and environmental contexts. Neocortical layer 1 (L1) is the main target of cortical and subcortical inputs that provide “top-down” information for context-dependent sensory processing. Although L1 is devoid of excitatory cells, it contains the distal “tuft” dendrites of pyramidal cells (PCs) located in deeper layers. L1 also contains a poorly characterized population of GABAergic interneurons (INs), which regulate the impact that different top-down inputs have on PCs. A poor comprehension of L1 IN subtypes and how they affect PC activity has hampered our understanding of the mechanisms that underlie contextual modulation of sensory processing. We used novel genetic strategies in male and female mice combined with electrophysiological and morphological methods to help resolve differences that were unclear when using only electrophysiological and/or morphological approaches. We discovered that L1 contains four distinct populations of INs, each with a unique molecular profile, morphology, and electrophysiology, including a previously overlooked IN population (named here “canopy cells”) representing 40% of L1 INs. In contrast to what is observed in other layers, most L1 neurons appear to be unique to the layer, highlighting the specialized character of the signal processing that takes place in L1. This new understanding of INs in L1, as well as the application of genetic methods based on the markers described here, will enable investigation of the cellular and circuit mechanisms of top-down processing in L1 with unprecedented detail. SIGNIFICANCE STATEMENT Neocortical layer 1 (L1) is the main target of corticocortical and subcortical projections that mediate top-down or context-dependent sensory perception. However, this unique layer is often referred to as “enigmatic” because its neuronal composition has been difficult to determine. Using a combination of genetic, electrophysiological, and morphological approaches that helped to resolve differences that were unclear when using a single approach, we were able to decipher the neuronal composition of L1. We identified markers that distinguish L1 neurons and found that the layer contains four populations of GABAergic interneurons, each with unique molecular profiles, morphologies, and electrophysiological properties. These findings provide a new framework for studying the circuit mechanisms underlying the processing of top-down inputs in neocortical L1.
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TL;DR
Using genetic, electrophysiological, and morphological methods in mouse barrel cortex, this study identifies four distinct GABAergic interneuron populations in neocortical layer 1: NDNF/NPY NGFCs, NDNF/non-NPY canopy cells, α7 nAChR cells, and VIP cells. The previously overlooked canopy cells account for ~40% of L1 interneurons and differ from NGFCs in morphology and connectivity.
Key findings
- L1 contains four molecularly defined interneuron populations: NDNF/NPY (NGFCs), NDNF/non-NPY (canopy cells), α7 nAChR cells, and VIP cells. NDNF labeling captured ~70% of L1 INs (66.8 ± 1.3%, n = 4 mice); NDNF/NPY cells were ~40% of the NDNF population (~30% of L1), NDNF/non-NPY cells ~60% (~40% of L1), and non-NDNF cells ~30% of L1, split into ~30% VIP (~10% of L1) and ~70% α7 cells (~20% of L1).
- Electrophysiologically, NGFCs were late-spiking (time to first spike 750.1 ± 28.6 ms; adaptation index 1.01 ± 0.02), VIP cells had high input resistance (351.1 ± 21.1 MΩ) and strong adaptation (0.44 ± 0.05), and α7 cells had a prominent near-threshold depolarizing hump (17.3 ± 0.5 mV) and larger sag (21.5 ± 1.6%). Canopy cells were non-LS with moderate adaptation (0.83 ± 0.02).
- Morphologically, NGFC and canopy axons were largely confined to L1, but canopy axons were biased to the upper half of L1 (L1a p = 3.3e-4; L1b p = 5.8e-4), whereas NGFC axons occupied the whole layer. α7 and VIP cells had descending collaterals; α7 cells were multipolar and VIP cells bipolar (p = 0.0047), with different soma sizes (p = 0.0012).
- Connectivity differed: NGFC→L2 PC connection probability was 72% (13/18) versus 18% for canopy cells (8/45; p = 7.2e-5); NGFC IPSPs were larger (p = 7.6e-4) and had a significant GABA_B component (p = 0.031), while canopy IPSPs did not. NGFC→canopy IPSPs were stronger than canopy→NGFC IPSPs (p = 0.012).
Methods
- Genetic labeling and histology in male and female mice (P21–P53; mean age P30.3 ± 0.3), using NPY-hrGFP, NDNF-ires-Cre, Htr3a-ires-Flpo, VIP/CCK lines, viral tdTomato reporter, FISH/IHC, and α-bungarotoxin labeling.
- Whole-cell current-clamp recordings in barrel field of primary somatosensory cortex slices, with biocytin filling for post hoc morphology; paired recordings between L1 INs and L2 PCs; intrinsic properties measured from 1-s current injections.
- Unsupervised cluster analysis (Ward’s method) on 82 cells using 11 electrophysiological parameters; statistics included Kruskal-Wallis with Dunn’s/Šidák correction, Mann-Whitney U, Fisher’s exact, and Wilcoxon signed-rank tests.
Limitations
- Stated: further studies may reveal additional diversity within the described groups; it is not yet clear how transcriptomic clustering corresponds to specific functional cell properties; some comparative area data are not shown.
- Stated/evident: some cells lacked complete electrophysiological analysis (n values are minimum), and cells could be used either for reconstructions or α-btx staining, not both; liquid junction potential was not corrected and cells with access resistance >35 MΩ were excluded.
- Evident: findings are from in vitro mouse barrel cortex slices at P21–P53, so age/area generality and in vivo circuit or behavioral roles are not established here; no sex-specific analyses are reported despite use of male and female mice.
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“including a previously overlooked IN population (named here”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Abstract
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“including a previously overlooked IN population (named here”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Abstract
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“We discovered that L1 contains four distinct populations of INs, each with a unique molecular profile, morphology, and electrophysiology, including a previously overlooked IN population (named here”
- Also stated in: § Significance Statement · plain
“We identified markers that distinguish L1 neurons and found that the layer contains four populations of GABAergic interneurons, each with unique molecular profiles, morphologies, and electrophysiological properties.”
- Also stated in: § Significance Statement · plain
“We identified markers that distinguish L1 INs and found that L1 contains four IN populations, each with unique molecular profiles, morphologies, and electrophysiological properties.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Abstract
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“Remarkably, although sparse, cells strongly labeled for ␣7 nAChRs (hereafter called ␣7 cells) were almost exclusively restricted to L1 (Fig. 2).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“We found that Ͼ90% of the GFP-positive cells in L1 (n ϭ 153/165 recorded NPYϩ cells; Fig. 1B) had the LS firing pattern characteristic of NGFCs.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“Conversely, LS cells were rarely observed among GFPnegative INs (n ϭ 25/183 recorded NPYcells; Fig. 1B).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“Therefore, the molecular analysis defined four distinct L1 IN populations: NDNF/NPY, NDNF/non-NPY, ␣7, and VIP (Fig. 2G).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“The remaining INs in L1 (ϳ30%) did not express NDNF.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“We identified markers that distinguish L1 neurons and found that the layer contains four populations of GABAergic interneurons, each with unique molecular profiles, morphologies, and electrophysiological properties.”
- Also stated in: § Significance Statement · plain
“We identified markers that distinguish L1 INs and found that L1 contains four IN populations, each with unique molecular profiles, morphologies, and electrophysiological properties.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Significance Statement
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“We found that neurons in each molecularly defined L1 group had a characteristic morphology (Figs. 4, 5).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“We discovered that L1 contains four distinct populations of INs, each with a unique molecular profile, morphology, and electrophysiology, including a previously overlooked IN population (named here”
- Also stated in: § Significance Statement · plain
“We identified markers that distinguish L1 neurons and found that the layer contains four populations of GABAergic interneurons, each with unique molecular profiles, morphologies, and electrophysiological properties.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Abstract
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“The axon of the canopy cells extends further from the soma (Fig. 6D; p ϭ 0.021; Mann-Whitney U test) and is less tortuous than the axon of NGFCs (Fig. 6E; p ϭ 0.0024; Mann-Whitney U test).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“The experimental observer could distinguish cell types with a high degree of certainty using a few key properties that distinguished among cells: the long delay to first spike and lack of adaptation at threshold of NDNF/NPY cells, the active depolarizing hump at threshold for the ␣7 cells, the presence of onset spikes at threshold without an active depolarizing hump for the NDNF/non-NPY cells, and”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“Using ISH, we confirmed that cortical NDNF expression is highly enriched in L1 INs (Fig. 2), having no overlap with the other major IN classes (PV, SST, and VIP).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“L1 VIP cells resemble the bipolar VIP INs in L2/3, with a descending axon that projects through the cortical column (Lee et al., 2010;Pro ¨nneke et al., 2015).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
What the sources say
- Not checked yetcites Lee et al., 2010
- Not checked yetcites Pro ¨nneke et al., 2015
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“By incorporating the NPY-hrGFP reporter into this approach, we found that the NPY population comprised a subset of L1 INs within the NDNF population such that NDNF cells could be divided into NPY-positive and NPY-negative groups (Fig. 2F ).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“The NDNF/non-NPY cells (hereafter called canopy cells, as explained below) resemble NGFCs in having an elongated horizontal axonal arbor largely confined to L1; however, they show several significant morphological differences from NGFCs.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“The dendritic arbor of the canopy cells is wider than that of NGFCs (Fig. 6A; p ϭ 0.0023; Mann-Whitney U test) and branches less (Fig. 6B; p ϭ 0.0072, respectively; Mann-Whitney U test).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“Most NDNF/NPY cells (92% in the present dataset) had a LS firing pattern near threshold and non-adapting or even accelerating repetitive firing;”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“NDNF/NPY cells (hereafter called NGFCs) had a NGFC morphology with short dendrites and a wider dense axonal arbor, which differs from NGFCs in other layers by often extending horizontally across several columns, as described previously (Hestrin and Armstrong, 1996;Zhou and Hablitz, 1996b;Kubota et al., 2011;Jiang et al., 2013Jiang et al., , 2015;;Tremblay et al., 2016).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
What the sources say
- Not checked yetcites Hestrin and Armstrong, 1996
- Not checked yetcites Zhou and Hablitz, 1996b
- Not checked yetcites Kubota et al., 2011
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“Interestingly, we also found that the axonal arbor of the two NDNF populations had a different distribution within L1: whereas the axon of NGFCs tends to occupy the whole layer, the axon of the canopy cells is strongly biased toward the upper half of L1, and is rarely found in L2 (Fig. 4C,D; L1a: p ϭ 3.3e-4; L1b: p ϭ 5.8e-4; Mann-Whitney U test).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“Approximately 30% of non-NDNF INs (and thus 10% of L1) were VIP cells, a marker that did not overlap with NDNF (Fig. 2C)”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“VIP cells in L1 have very high input resistances and adapt the most (input resistance: 351.1 M⍀ Ϯ 21.1 compared with 141.9 Ϯ 6.6 and 141.6 Ϯ 10.8 for the NDNF/non-NPY and ␣7 populations, respectively; adaptation index: 0.44 Ϯ 0.05 compared with 0.83 Ϯ 0.02 and 0.60 Ϯ 0.03 for the NDNF/non-NPY and ␣7 populations respectively; for statistics, see Table 3)”
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“NDNF/NPY INs account for ϳ40% of the NDNF population (mean Ϯ SEM ϭ 40.8 Ϯ 0.7%, n ϭ 4 mice and thus ϳ30% of L1)”
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“Furthermore, peak axonal density is ϳ65% larger (Fig. 6G; p ϭ 0.0152; Mann-Whitney U test) and the interbouton distance is smaller (Fig. 6F; p ϭ 0.0016; Mann-Whitney U test) for NGFCs, resulting in a twofold difference in bouton density for the two cell types.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“and the NDNF/non-NPY population for 60% (and thus ϳ40% of L1).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
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“The descending axonal collaterals of L1 VIP cells branch in L5A, a cortical sublayer that often receives projections from similar sources as L1 and then continue into L5B, often reaching layer 6 (Figs. 4, 5).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“Inset shows the magnified somatodendritic profile of the ␣7 and VIP cells showing that the ␣7 cell is multipolar and the VIP cell is bipolar.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Sublaminar structure of layer 1
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“Consistent with observations in other studies, we find robust unitary GABA B re-sponses in L1 NGFC connections with L2 PCs, representing a significant proportion of the PSP elicited by NGFC stimulation (Fig. 8 B, E; p ϭ 0.031; Wilcoxon signed-rank test).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > NGFC and canopy cells differ in connectivity
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“Like VIP cells, ␣7 cells have one or more vertically descending axonal collaterals that go deep into the column.They usually branch in L5A, but often terminate there, in contrast to VIP cells (Figs. 4A, 5).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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“The two NDNF populations have similar morphologies but very distinct electrophysiological properties.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
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None of the sources cited for this claim have been checked yet.
In the paper
“Conversely, although L1 VIP cells resemble bipolar VIP cells in L2-6, their bipolar dendrite is oriented horizontally (Fig. 4), whereas the dendritic trees of bipolar VIP INs in other layers are narrow and oriented vertically, crossing several layers in either direction (Lee et al., 2013;Pro ¨nneke et al., 2015).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Discussion
What the sources say
- Not checked yetcites Lee et al., 2013
- Not checked yetcites Pro ¨nneke et al., 2015
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The two NDNF populations, NGFCs and canopy cells, also differ in their connectivity to L2 PCs and each other, supporting the notion that they represent distinct IN subtypes (Figs. 8, 9).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > NGFC and canopy cells differ in connectivity
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“NGFCs and canopy cells were reciprocally connected and the probability of detecting connections was high in both directions (Fig. 9A).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > NGFC and canopy cells differ in connectivity
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Three additional non-NDNF cells were also confirmed as ␣7 nAChR-expressing, but only partial electrophysiological data were collectedfromthesecellsandtheywerethereforenotincludedinthisanalysis.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Sublaminar structure of layer 1
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Conversely, canopy cells and ␣7 neurons resemble each other electrophysiologically (Fig. 3) but are distinguishable morphologically.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > L1 IN populations have characteristic morphologies
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“NGFCs and VIP INs are present in other layers, but have unique properties in L1 of potential physiological significance.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Discussion
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Only IPSPs elicited by NGFCs had a significant GABA B component ( p ϭ 0.031, Wilcoxon signed-rank test).”
- Also stated in: § Sublaminar structure of layer 1 · plain
“showing a prominent GABA B component elicited by NGFCs, but not canopy cells.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Sublaminar structure of layer 1
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
- Also stated in: § Sublaminar structure of layer 1 · plain
None of the sources cited for this claim have been checked yet.
In the paper
“Previous studies of L1 INs agree that an important component of this population is neurogliaform cells (NGFCs), INs that mediate long-lasting GABA A and GABA B inhibition of PCs and have a late-spiking (LS) firing pattern when depolarized to near threshold membrane potentials (Chu et al., 2003;Tama ´s et al., 2003;Overstreet-Wadiche and McBain, 2015;Tremblay et al., 2016).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Significance Statement
What the sources say
- Not checked yetcites Chu et al., 2003
- Not checked yetcites Tama ´s et al., 2003
- Not checked yetcites Overstreet-Wadiche and McBain, 2015
boosteddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“VIP INs are the major population of L2/3 INs, accounting for 35% of the INs in these layers (Tremblay et al., 2016), but are infrequent in L1 (Lee et al., 2010).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
What the sources say
- Not checked yetcites Tremblay et al., 2016
- Not checked yetcites Lee et al., 2010
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“Furthermore, several studies have included a substantial proportion of unclassified cells (Table 1).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Significance Statement
What the sources say
- Not checked yetcites Table 1
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“This active depolarization resembles the Ca 2ϩ spike observed in thalamic relay neurons (Llina ´s and Jahnsen, 1982;Jahnsen and Llina ´s, 1984;McCormick and Huguenard, 1992) and is likely mediated by a similar Ca 2ϩ conductance because it is blocked by the T-channel blocker TTA-P2 (3 M; data not shown).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
What the sources say
- Not checked yetcites Llina ´s and Jahnsen, 1982
- Not checked yetcites Jahnsen and Llina ´s, 1984
- Not checked yetcites McCormick and Huguenard, 1992
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The intrinsic properties of cells with access resistances Ͼ35 M⍀ were not analyzed.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Slice preparation.
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“All recordings were performed in currentclamp conditions using the whole-cell configuration in brain slices and the liquid junction potential was not corrected.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Slice preparation.
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Therefore, most L1 INs are non-VIP 5HT3aR cells, a heterogeneous interneuron population with a poorly characterized diversity (Lee et al., 2010).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Four molecular IN populations in L1
What the sources say
- Not checked yetcites Lee et al., 2010
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, closer examination of these data indicated that a substantial fraction of cells clustered within the NDNF/Cxcl14 category were actually non-NDNF expressing and likely included the ␣7 cells reported here.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Discussion
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Comparative histological analysis indicates that the same populations are present in L1 across different cortical areas (data not shown), so our findings likely reflect general principles of L1 organization throughout the neocortex.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Discussion
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Inputs from canopy cells on PCs may thus be more subject to dendritic filtering and this may contribute at least in part to the apparent difference in synaptic strength recorded at the PC soma.”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > NGFC and canopy cells differ in connectivity
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“Consistent with this idea, a recent comparative analysis of IN single-cell transcriptomes reported broad conservation of molecularly defined IN subtypes across visual and premotor (ALM) cortices (Tasic et al., 2018).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Discussion
What the sources say
- Not checked yetcites Tasic et al., 2018
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Chandelier cells are enriched in L2 and contain a dendritic arborization mostly in L1, often reaching the cortical surface (Woodruff et al., 2011;Miyamae et al., 2017).”
§ Systems/Circuits Four Unique Interneuron Populations Reside in Neocortical Layer 1 > Discussion
What the sources say
- Not checked yetcites Woodruff et al., 2011
- Not checked yetcites Miyamae et al., 2017
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
The paper relies on this without support.
The NDNF-ires-Cre driver line specifically labels NDNF-expressing L1 INs.
“We then generated an NDNF-ires-Cre knock-in driver line (3Ј-UTR) and labeled NDNF-expressing INs via injection of a td-Tomato Cre reporter virus (AAV1.CAG.Flex.tdTomato.WPRE.bGH;Allen Institute 864) in the cortex.”
The paper relies on this without support.
The electrophysiological and morphological properties measured in acute slices reflect those of L1 INs in vivo.
“We performed whole-cell current clamp recordings in coronal slices of barrel cortex to characterize the intrinsic electrophysiological properties of each L1 population (mice aged P21-P53; mean age Ϯ SEM ϭ P30.3 Ϯ 0.3).”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Lamp5-MET-1 had APs with high upstroke/downstroke ratios and a neurogliaform-like morphology (Jiang et al., 2013; Jiang et al., 2015; Schuman et al., 2019); these cells were found primarily in L1 and L2/3 but also appeared in deeper cortical layers.”
From Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells (2020) · cites this paper as Schuman et al., 2019
Experimental — accuracy not yet measuredIn the citing paper
“We noted that each end of the spectrum resembled populations of L1 interneurons described in a recent study in barrel cortex (Schuman et al., 2019): the cells here with higher Npy expression have electrophysiology and morphology consistent with Ndnf+/Npy+ neurogliaform cells, and those at the other end have properties more similar to the “canopy cells” described in that study.”
From Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells (2020) · cites this paper as Schuman et al., 2019
Citations
Cites
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · cited 3×
“…System Atlas (GENSAT) Project, NINDS Contract # N01NS02331 to The Rockefeller University, VIP-ires-Cre (Jax stock #010908; Taniguchi et al., 2011), CCK-ires-Cre (Jax stock #012706; Taniguchi et al., 2011), Rosa26LSL-tdTomato (Ai9; Madisen et al., 2010), Rosa26FSF-LSL-tdTomato (Ai65(RCFL-tdT)-”
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572 · cited 1×
“To find markers that could help the segregation of L1 INs, we mined data from our own studies, as well as from the Allen Institute in situ hybridization (ISH) gene expression databases (Lein et al., 2007).”
MethodGABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033 · cited 1×
“Likewise, repetitive firing of SST INs has been shown to produce GABAB responses as well (Urban-Ciecko et al., 2015).”
BackgroundSelf-citationA resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex
Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsani, D., Fu, Y., Lu, J., Lin, Y., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.026 · Cited by 1,828 · cited 1×
“In the mouse, chandelier cells are highly enriched in the upper part of L2, near the border with L1 (Woodruff et al., 2009; Woodruff et al., 2011; Taniguchi et al., 2013), but are rarely seen in L1 proper (of the 409 cells that we recorded in L1, we only observed two fast-spiking cells; data not…”
BackgroundSelf-citationShared and distinct transcriptomic cell types across neocortical areas
Tasic, B., Yao, Z., Graybuck, L. T., Smith, K. A., Nguyen, T. N., Bertagnolli, D., Goldy, J., Garren, E., Economo, M. N., Viswanathan, S., et al. (2018) · Nature · doi:10.1038/s41586-018-0654-5 · Cited by 1,746 · cited 1×
“The concerted firing of several INs or high-frequency firing of a single interneuron are thought to release enough GABA to activate extrasynaptic receptors (Mody et al., 1994; Thomson et al., 1996; Kim et al., 1997; Thomson and Destexhe, 1999; Scanziani, 2000).”
BackgroundAdult mouse cortical cell taxonomy revealed by single cell transcriptomics
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., Levi, B., Gray, L. T., Sorensen, S. A., Dolbeare, T., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4216 · Cited by 1,714 · cited 4×
“This study expanded upon earlier work (Tasic et al., 2016) that delineated two primary NDNF populations, NDNF/Car4 and NDNF/Cxcl14, that may correspond to our L1 NGFC and canopy cell types, respectively.”
BackgroundMethodInfluentialThree groups of interneurons account for nearly 100% of neocortical GABAergic neurons
Rudy, B., Fishell, G., Lee, S., & Hjerling‐Leffler, J. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20853 · Cited by 1,420 · cited 1×
“Located in all cortical layers, 5HT3aR INs consist of two subgroups based on whether they express the neuropeptide VIP (Lee et al., 2010; Rudy et al., 2011; Tremblay et al., 2016).”
BackgroundSelf-citationWhole-Brain Imaging with Single-Cell Resolution Using Chemical Cocktails and Computational Analysis
Susaki, E. A., Tainaka, K., Perrin, D., Kishino, F., Tawara, T., Watanabe, T. M., Yokoyama, C., Onoe, H., Eguchi, M., Yamaguchi, S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.03.042 · Cited by 1,352 · cited 1×
“After labeling, slices were moved to cold 4% PFA for 3–12 h and then stored in 30% sucrose with 0.1 M PB. Slices were thoroughly washed with 0.1 M PB and then moved to CUBIC #1 tissue clearing solution (Susaki et al., 2014, 2015) for 2 d.”
MethodInfluentialTamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K., & Kaneko, T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10905 · Cited by 1,277 · cited 3×
“, 2009), GAD67-GFP (Riken BRC stock #RBRC03674; Tamamaki et al., 2003), vasoactive intestinal peptide (VIP)-EGFP (MMRRC stock #031009-UCD; The Gene Expression Nervous System Atlas (GENSAT) Project, NINDS Contract # N01NS02331 to The Rockefeller University, VIP-ires-Cre (Jax stock #010908; Taniguchi et al.”
BackgroundMethodTop-down influences on visual processing
Gilbert, C. D., & Li, W. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3476 · Cited by 1,224 · cited 19×
“For example, a single FS IN in auditory cortex can produce GABAB responses on connected PCs when stimulated at 80 Hz (Oswald et al., 2009).”
BackgroundInfluential
Cited by
Sorted by citations
Items 201–219 of 219
Moreno, C., Riquelme, D., Cornejo, C., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.28.702118
Presynaptic control of top-down signaling in neocortical layer 1Preprint
Bonekamp, K. E., Ratz, M. L., Gillie, G. R., Xiong, L., Sebek, M., & Crandall, S. R. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.31.703032
Circuit organization of the forelimb-related M2-to-M1 corticocortical pathway in the mousePreprint
Richevaux, L., Fischer, R., Baid, M., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.03.703577
Moreno, C., Riquelme, D., Cornejo, C., Leyton, P., & Leiva‐Salcedo, E. (2026) · Biological Research · doi:10.1186/s40659-026-00673-2
Assembling layer 1 of the neocortex : roles of Cajal-Retzius cells
Genescu, I. (2020) · theses.fr (ABES) · doi:10.70675/3fe1b21cz5c6bz4150z94e6zd77163aba0ad
Altérations de la connectivité corticale au cours de périodes critiques du développement
Druart, M. (2020) · theses.fr (ABES) · doi:10.70675/b4f48d73za850z42b2z8dadzfad47d4f0a69
The role of the α7 nicotinic acetylcholine receptor in a model of amyloid pathology
Santos, D. G. (2024) · theses.fr (ABES) · doi:10.70675/b3ed4de5zcd9ez4421za129z0a05130d86b9
Martinez, M. (2025) · theses.fr (ABES) · doi:10.70675/d05e33fcz2cd4z45d4zbe74z5e57fadd4292
Richardson, A., Mercier, M. S., Shimoda, Y., Graham, R., Leite, M., Garcia, A., Muller, M., Bond, S. A., Grodzdanova, M., Wu, Q., et al. (2026) · EBioMedicine · doi:10.1016/j.ebiom.2026.106362
Layer 1 NDNF interneurons modulate thalamocortical input to the auditory cortex
Tao, J., Chen, Y., Polat, M., Li, S. C., Chen, X., & Zhao, Z. (2026) · iScience · doi:10.1016/j.isci.2026.116836
Kopach, O., Reynolds, J. R., Jensen, T. P., Zheng, K., Savtchenko, L. P., & Rusakov, D. A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.2139/ssrn.7135125
Banovac, I., Baković, M., Mayer, D., Sedmak, D., & Petanjek, Z. (2026) · Journal of Anatomy · doi:10.1111/joa.70223
A thalamocortical circuit encoding deviations from sensory history
Leow, Y. N., Natesan, A., Barlowe, A. R., Ährlund‐Richter, S., Luo, T., Jazayeri, M., & Sur, M. (2026) · Science · doi:10.1126/science.aeg4720
GABAergic interneurons in local circuits of primate prefrontal cortex
Pommer, S., Lewis, D. A., Krienen, F. M., Feyerabend, M., Rico, B., Tripathy, S., Martínez-Trujillo, J., Burgos, G.-G., Neef, A., & Staiger, J. F. (2026) · Biological Psychiatry · doi:10.1016/j.biopsych.2026.09.012 · Cited by 2
Most Early‐Born Subplate Neurons Persist as Layer 6b Neurons in the Adult Mouse Neocortex
Sugita, Y., Moriya‐Ito, K., Hanashima, C., & Ohtaka‐Maruyama, C. (2026) · The Journal of Comparative Neurology · doi:10.1002/cne.70200
Metadata
- Authors
- Schuman, B., Machold, R. P., Hashikawa, Y., Fuzik, J., Fishell, G. J., & Rudy, B.
- Affiliations
- New York University (US)
- Harvard University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-11-09
- Volume
- 39
- Issue
- 1
- Pages
- 125-139
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6325270
- OpenAlex
- W2900330446
- Semantic Scholar
- 70ba50776b5fd3e4bfed41386e838ac7bd15a885
- Cited by
- 184
- References
- 88
- Citations by year
- 2026: 13 · 2025: 34 · 2024: 25 · 2023: 25 · 2022: 25 · 2021: 24 · 2020: 28 · 2019: 10
- FWCI
- 7.06
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (UG3MH120096, T32MH096331, R37MH071679)
- National Institute of Neurological Disorders and Stroke (R01NS107257, P01NS074972, R01NS110079, F31NS106793, R01NS081297)
- 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 › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- GABAergic interneurons, interneuron subtypes, top-down processing, neuronal morphology, electrophysiological properties, corticocortical connections, sex differences
- MeSH terms
- Animals, Dendrites, Female, gamma-Aminobutyric Acid, Interneurons, Male, Mice, Transgenic, Pyramidal Cells, Patch-Clamp Techniques, Neocortex, Mice, Electrophysiological Phenomena
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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