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Developmental diversification of cortical inhibitory interneurons
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Abstract
Diverse subsets of cortical interneurons have vital roles in higher-order brain functions. To investigate how this diversity is generated, here we used single-cell RNA sequencing to profile the transcriptomes of mouse cells collected along a developmental time course. Heterogeneity within mitotic progenitors in the ganglionic eminences is driven by a highly conserved maturation trajectory, alongside eminence-specific transcription factor expression that seeds the emergence of later diversity. Upon becoming postmitotic, progenitors diverge and differentiate into transcriptionally distinct states, including an interneuron precursor state. By integrating datasets across developmental time points, we identified shared sources of transcriptomic heterogeneity between adult interneurons and their precursors, and uncovered the embryonic emergence of cardinal interneuron subtypes. Our analysis revealed that the transcription factor Mef2c, which is linked to various neuropsychiatric and neurodevelopmental disorders, delineates early precursors of parvalbumin-expressing neurons, and is essential for their development. These findings shed new light on the molecular diversification of early inhibitory precursors, and identify gene modules that may influence the specification of human interneuron subtypes.
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“Heterogeneity within mitotic progenitors in the ganglionic eminences is driven by a highly conserved maturation trajectory, alongside eminence-specific transcription factor expression that seeds the emergence of later diversity.”
- Also stated in: § Introduction · plain
“Within mitotic progenitors, we found a highly conserved maturation trajectory, accompanied by eminence-specific transcription factor expression that seeds the emergence of later cell diversity.”
§ Developmental diversification of cortical inhibitory interneurons > Abstract
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“Upon becoming postmitotic, progenitors diverge and differentiate into transcriptionally distinct states, including an interneuron precursor state.”
§ Developmental diversification of cortical inhibitory interneurons > Abstract
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In the paper
“Our analysis revealed that the ASD-associated transcription factor Mef2c delineates early Pvalb-precursors, and is essential for their development.”
- Also stated in: § Diversity emerges from a common precursor state · plain
“the transcription factor Mef2c was among the genes discriminating early Pvalb-precursors from other MGE-derived interneuron types”
§ Developmental diversification of cortical inhibitory interneurons > Abstract
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“conditional deletion of Mef2c in inhibitory neurons led to a specific loss of Pvalb-interneurons by P20 in cortical layers 2-6”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
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“when we performed the unsupervised branching analysis only in mitotic progenitors, we found no evidence for the specification of distinct interneuron fates”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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“a second group of branches (i.e. precursor state 2) expressed known projection neuron marker genes (i.e. Isl1, Ebf1; Fig. 3E; Supplementary Table 4)”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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“we performed a differential expression analysis and found a small number of transcription factors enriched in mitotic progenitors within particular eminences”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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In the paper
“As expected, neurons born at these sequential timepoints were distributed progressively along the MT timeline (Fig. 1H, Extended Data Fig. 1).”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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“we found that, as expected20, more than 80% of Dlx6a-Cre fate mapped cortical cells at E18.5 mapped to precursor state 1, based on their expression of canonical regulators of interneuron development”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
What the sources say
- Not checked yetcites [20] Wichterle, H ., Turnbull, D. H ., Nery, S ., Fishell, G. & Alvarez-Buylla, A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128, 3759–3771 (2001) source
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“even though branched trajectories for each eminence were calculated independently, branch gene expression markers were highly correlated across eminences”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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In the paper
“By integrating datasets across developmental timepoints, we identified shared sources of transcriptomic heterogeneity between adult interneurons and their precursors, revealing the embryonic emergence of interneuron cardinal subtypes.”
§ Developmental diversification of cortical inhibitory interneurons > Abstract
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“the number of conserved DE genes grow over time. Same analysis for Pvalb vs. Sst subsets (Middle), and Vip vs. Id2 subsets (Right).”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“Developmental progression and cell cycle were the primary sources of transcriptional variance in these progenitors (Supplementary Methods), with maturation proportionally explaining six-fold more variance compared to eminence-of-origin”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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In the paper
“Genetic fate mapping using Lhx8-Cre/cerulean demonstrates that MGE branch three precursors give rise to the entire breadth of cholinergic projection (Globus Pallidus and Nucleus Basalis) and interneuron (striatum) populations.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“Mitotic cells fall within a homogeneous point cloud, with low variance on PC1 and PC2, showing no evidence of fate bifurcation.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“the vast majority of Dlx6a-Cre;RCEloxP positive E18.5 cortical cells map to the interneuron precursor state, and are split between MGE and CGE-derived precursors.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“The cumulative longitudinal use of a constitutive Cre driver also results in extensive labeling of cortical interneurons due to transient expression within this population.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“By E18, all cardinal types of interneurons could be identified, and additional subtypes appeared to be transcriptionally specified as well”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
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“In-situ hybridization (ISH) confirmed that these waves describe the sequential expression of stem-cell (e.g. Nes), proneural (e.g., Ascl1), and neurogenic genes (e.g. Dcx; Fig. 2C), roughly correlating with the spatiotemporal progression from the VZ to the mantle zone (MZ)”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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In the paper
“Of all cells, 3,432 GABAergic interneurons were easily identified by the expression of Gad1 and depletion of Slc17a7, and were selected for downstream analysis.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“The third group of branches (i.e. precursor state 3) exhibited weaker correlation across eminences, with the transcription factor Lhx8 representing a marker gene for the MGE Branch 3”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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In the paper
“Integrated analysis with the P56 dataset results in clearer separation, and enables us to map developmental precursors to adult subtypes.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“Based on this alignment, P10 cells exhibited strong evidence of transcriptomic separation beyond cardinal types, (Fig. 4B), including clear segregation between Sst Martinotti versus non-Martinotti (X94), Vip bipolar versus multipolar, and Id2 neurogliaform versus non-neurogliaform interneuron subtypes”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
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In the paper
“We first observed evidence of clear fate bifurcations as cells become postmitotic, and precursors from all GEs branched into distinct precursor states”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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“we identified rare populations that did not express canonical interneuron (IN) markers, likely representing false positives from FACS.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“tSNE visualization and graph-based clustering of the 3,432 GABAergic cells reveals 14 clusters, which could be broadly grouped into cardinal types based on the expression of canonical markers”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“While we did observe computational evidence of branching, this does not represent fate bifurcations as we observed in postmitotic cells.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“we observed a separation of Pvalb- and Sst-precursor cells within the E13.5 postmitotic populations (Fig. 4D), and identified transcriptomic markers that were conserved into adulthood”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
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In the paper
“branching trajectories represented the most significant source of variation in these cells, with an increasing contribution attributable to eminence of origin compared to mitotic progenitors”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
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In the paper
“The trend overall shows that genes with peak expression at low MS tend to have higher expression in the VZ, and as MS rank increases the expression pattern shifts to the subventricular zone (SVZ) and then to the MZ”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
What the sources say
- Not checked yetcites [31] Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010) source
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In the paper
“A minority of E13.5 cells also mapped to Vip and Id2 subsets, but conserved transcriptomic markers did not pass statistical significance until E18.5”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
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In the paper
“Genetic ‘fate-mapping’ using Lhx8-Cre suggested that these neurons account for the majority, if not all of the cholinergic projection and interneuron populations within the nucleus basalis, medial septum, and striatum, respectively, as well as the majority of Pvalb-positive projection neurons in the globus pallidus5,6”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
What the sources say
- Not checked yetcites [5] Nóbrega-Pereira, S . et al. Origin and molecular specification of globus pallidus neurons. J. Neurosci. 30, 2824–2834 (2010) source
- Not checked yetcites [6] Zhao, Y . et al. The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc. Natl Acad. Sci. USA 100, 9005–9010 (2003) source
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In the paper
“These components reflect our previously defined maturation trajectory, with DMC1 separating mitotic cells (left).”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“Our Lhx6-GFP-negative dataset contains both mitotic and postmitotic cells from the CGE and diffusion map analysis shows our previously defined maturation trajectory.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“the clear emergence of Sst, Vip and Id2 subtypes was apparent for a subset of cells at E18.5 (Extended Data Figure 8), but we were unable to clearly subdivide Pvalb neurons by P10, in accordance with their late maturation28.”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
What the sources say
- Not checked yetcites [28] Harrington, A. J . et al. MEF2C regulates cortical inhibitory and excitatory synapses and behaviors relevant to neurodevelopmental disorders. eLife 5, 140 (2016) source
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In the paper
“Diffusion map analysis of these cells returned only two significant principal components, with no evidence of further structure.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“observed that MT recapitulated known dynamics associated with neuronal maturation (Fig. 1E) while also segregating GE cells into ‘mitotic’ and ‘postmitotic’ phases”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
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In the paper
“This diverse group of neurons is developmentally derived from progenitors residing in embryonic proliferative zones known as the medial, caudal and lateral ganglionic eminences (MGE, CGE, LGE, respectively)1.”
§ Developmental diversification of cortical inhibitory interneurons > Introduction
What the sources say
- Not checked yetcites [1] Kepecs, A. & Fishell, G. Interneuron cell types are fit to function. Nature 505, 318–326 (2014) source
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“The MGE and CGE are known to produce non-overlapping types of cortical interneurons16.”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
What the sources say
- Not checked yetcites [16] Rudy, B ., Fishell, G ., Lee, S. & Hjerling-Leffler, J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011) source
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In the paper
“Supplementing these more general programs are the eminence-specific genes that, for example, may direct the axons of parvalbumin cortical interneurons to form perisomal baskets and the efferents of somatostatin cortical interneurons to reliably target dendrites.”
§ Developmental diversification of cortical inhibitory interneurons > DISCUSSION
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In the paper
“Cells expressing both genes are likely projection neuron precursors that have recently been described in the CGE21, but whose progeny is not captured in the mouse visual cortex dataset.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
What the sources say
- Not checked yetcites [21] Frazer, S . et al. Transcriptomic and anatomic parcellation of 5-HT3AR expressing cortical interneuron subtypes revealed by single-cell RNA sequencing. Nat. Commun. 8, 14219 (2017) source
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In the paper
“To avoid the possibility of FACS false negative MGE cells contaminating our Lhx6-GFP-negative dataset, we clustered the postmitotic cells from this dataset, and filtered out three rare clusters where Lhx6 mRNA expression was detected in more than 20% of cells”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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In the paper
“We manually dissected the embryonic day (E)13.5 MGE or E14.5 CGE and LGE from wild type mouse embryos, timepoints corresponding to peak neurogenesis in these structures7,8”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
What the sources say
- Not checked yetcites [7] Inan, M ., Welagen, J. & Anderson, S. A. Spatial and temporal bias in the mitotic origins of somatostatin- and parvalbumin-expressing interneuron subgroups and the chandelier subtype in the medial ganglionic eminence. Cereb. Cortex 22, 820–827 (2012) source
- Not checked yetcites [8] Miyoshi, G . et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582–1594 (2010) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. 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
“Thus, our data reveal how postmitotic pan-eminence transcriptional programs (precursor states) emerge, and in parallel, eminence-specific transcriptional programs escalate.”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
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In the paper
“Genome-wide association studies have linked mutations in this gene to Alzheimer’s, schizophrenia, and other neurodevelopmental disorders29.”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Diversity emerges from a common precursor state
What the sources say
- Not checked yetcites [29] Habib, N . et al. Massively parallel single-nucleus RNA-seq with DroNc-seq. Nat. Methods 14, 955–958 (2017) source
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In the paper
“These cells have been recently described as being present in the cortical white matter and likely represent projection neuron precursors21.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
What the sources say
- Not checked yetcites [21] Frazer, S . et al. Transcriptomic and anatomic parcellation of 5-HT3AR expressing cortical interneuron subtypes revealed by single-cell RNA sequencing. Nat. Commun. 8, 14219 (2017) source
Strength:hedged· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably 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
“We performed latent variable regression to mitigate heterogeneity resulting from cell-cycle state10,11 (Extended Data Fig. 1), preventing subsequent analysis from being dominated by mitotic phase-specific gene expression”
§ Developmental diversification of cortical inhibitory interneurons > RESULTS > Transcriptional profiling of GE cells
What the sources say
- Not checked yetcites [10] Buettner, F . et al. Computational analysis of cell-to-cell heterogeneity in single-cell RNA-sequencing data reveals hidden subpopulations of cells. Nat. Biotechnol. 33, 155–160 (2015) source
- Not checked yetcites [11] Tirosh, I . et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189–196 (2016) source
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In the paper
“Therefore, our FlashTag maturation trajectory serves as complementary validation of our Drop-seq maturation trajectory, and exhibits strong association with biological time.”
§ Developmental diversification of cortical inhibitory interneurons > Extended Data
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The paper relies on this without support.
The genetic programs that drive interneuron fate specification and maintenance are not well understood.
“the genetic programs driving interneuron fate specification and maintenance are not well understood”
The paper relies on this without support.
It remains unclear how early sources of heterogeneity generate the vast diversity of adult interneurons.
“it remains unclear how these early sources of heterogeneity generate the vast diversity of adult interneurons”
Claims other papers make about this one
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In the citing paper
“a contemporaneous study based on a different scRNA-seq approach found no evidence for early embryonic specification of interneurons into specific cell types”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Mayer et al., 2018
In the citing paper
“The cardinal identity of a cell is probably already instilled at the postmitotic stage during development9,61,62,63,64, and its subsequent phenotypic differentiation and expression are regulated by extrinsic signals such as cell interactions and neural activity.”
From The diversity of GABAergic neurons and neural communication elements (2019) · cites this paper as [61]
In the citing paper
“Cortical excitatory neuron transcriptomes may be more heterogeneous due to their developmental origin spread across the dorsal telencephalon, compared with GABAergic populations that originate in the ganglionic eminences and migrate to cortex (Mayer et al., 2018).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Mayer et al., 2018
In the citing paper
“scRNA-seq reveals how neuronal and glial cell type identities emerge in developing mouse (Mayer et al., 2018; Telley et al., 2019; Tiklová et al., 2019) and human brain (Li et al., 2018; Nowakowski et al., 2017; Pollen et al., 2015), and even across whole organisms (Farrell et al., 2018).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Mayer et al., 2018
In the citing paper
“Lhx6–a transcription factor–participates in cell fate determination of MGE types, whereas Lamp5+ neocortical interneurons come from the CGE35.”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [35]
In the citing paper
“(and both are expressed in the cortical Lamp5+ Lhx6+ type)”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [35]
In the citing paper
“In mouse mature cortical interneurons, Id2 and Lamp5 are expressed in nearly identical populations35”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [35]
In the citing paper
“Developmentally, Sst+and Pavlb+ originate from the medial ganglionic eminence (MGE), while the Vip+ originate from the caudal ganglionic eminence (CGE)15.”
From Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction (2019) · cites this paper as [15]
In the citing paper
“and are likely the remaining non-MGE origin cells (arising from CGE and/or POA)14–16”
From Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction (2019) · cites this paper as [15]
In the citing paper
“For example, Mayer et al (2018) fit a negative binomial model to count data, using technical covariates such as the read depth and the number of counts per gene to fit the model parameters.”
From Current best practices in single-cell RNA-seq analysis: a tutorial (2019) · cites this paper as Mayer et al, 2018
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Metadata
- Authors
- Mayer, C., Hafemeister, C., Bandler, R. C., Machold, R., Batista Brito, R., Jaglin, X., Allaway, K., Butler, A., Fishell, G., & Satija, R.
- Affiliations
- Broad Institute (US)
- New York Genome Center (US)
- NYU Langone Health (US)
- Harvard University (US)
- Corresponding author
- Fishell, Gord
- Satija, Rahul
- ORCID
- Venue
- Nature
- Published
- 2018-03-05
- Volume
- 555
- Issue
- 7697
- Pages
- 457-462
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6052457
- OpenAlex
- W2791731597
- Semantic Scholar
- 7450ce01a65bcf74dd0dabd3df9b6cf350b4401b
- Cited by
- 492
- References
- 42
- Citations by year
- 2026: 39 · 2025: 43 · 2024: 50 · 2023: 53 · 2022: 65 · 2021: 76 · 2020: 73 · 2019: 59 · 2018: 34
- FWCI
- 22.24
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Science Foundation (1342536)
- Simons Foundation (P01 NS074972)
- Deutsche Forschungsgemeinschaft
- National Institutes of Health (NIH DP2, 1dp2hg009623-01, MH071679, NS074972)
- National Institute of Mental Health (F30MH114462, R01MH111529, R01MH071679, R37MH071679)
- National Human Genome Research Institute (DP2-HG-009623)
- National Institute of General Medical Sciences (T32GM007308)
- National Institute of Neurological Disorders and Stroke (P01NS074972, F31NS103398, R01NS039007, R01NS081297)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- cortical interneurons, MEF2C, parvalbumin neurons, ganglionic eminence, transcriptional heterogeneity, interneuron subtypes, developmental trajectories, transcription factors, neuropsychiatric disorders, mouse embryo
- MeSH terms
- Animals, Cell Differentiation, Embryo, Mammalian, Female, Ganglia, Humans, Interneurons, Male, Mitosis, Neural Inhibition, Parvalbumins, Visual Cortex, RNA, Small Cytoplasmic, Gene Expression Profiling, Mice, Single-Cell Analysis, MEF2 Transcription Factors
About these checks
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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