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Conserved cell types with divergent features in human versus mouse cortex
Open accessPublished version of a preprint
Abstract
Elucidating the cellular architecture of the human cerebral cortex is central to understanding our cognitive abilities and susceptibility to disease. Here we used single-nucleus RNA-sequencing analysis to perform a comprehensive study of cell types in the middle temporal gyrus of human cortex. We identified a highly diverse set of excitatory and inhibitory neuron types that are mostly sparse, with excitatory types being less layer-restricted than expected. Comparison to similar mouse cortex single-cell RNA-sequencing datasets revealed a surprisingly well-conserved cellular architecture that enables matching of homologous types and predictions of properties of human cell types. Despite this general conservation, we also found extensive differences between homologous human and mouse cell types, including marked alterations in proportions, laminar distributions, gene expression and morphology. These species-specific features emphasize the importance of directly studying human brain.
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“As a third example of the great elaboration and specialization associated with consciousness, the more-advanced animal brains have the largest numbers of neuron types, with highly complex interactions (Strausfeld, 2012; Feinberg and Mallatt, 2016a; Hodge et al., 2019).”
From Phenomenal Consciousness and Emergence: Eliminating the Explanatory Gap (2020) · cites this paper as Hodge et al., 2019
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“nuclei were sorted using a standard gating strategy to exclude multiplets24”
From Integrated multimodal cell atlas of Alzheimer’s disease (2024) · cites this paper as [24]
In the citing paper
“8 out of 14 modules showed greater intra-module correlation than a comparable random gene set in the adult human brain dataset from Hodge et al (30) (Fig. 4B).”
From In vivo Perturb-Seq reveals neuronal and glial abnormalities associated with autism risk genes (2020) · cites this paper as [30]
In the citing paper
“In addition, multiplex FISH is already being used to measure the proportions of transcriptomic types within a given brain tissue (Hodge et al., 2019; Moffitt et al., 2018; Zhang et al., 2020).”
From Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells (2020) · cites this paper as Hodge et al., 2019
In the citing paper
“Single-cell RNA-sequencing (scRNA-seq) studies have systematically characterized and classified cell types in individual regions of isocortex and hippocampus”
From A taxonomy of transcriptomic cell types across the isocortex and hippocampal formation (2021) · cites this paper as Hodge et al., 2019
In the citing paper
“The application of single-cell RNA sequencing (scRNA-seq) to the neocortex and other brain regions has revealed a complex but tractable hierarchical organization of transcriptomic cell types that are consistent overall with knowledge from decades of anatomical, physiological and developmental studies but with an unmatched level of granularity7–11.”
From A multimodal cell census and atlas of the mammalian primary motor cortex (2021) · cites this paper as [10]
In the citing paper
“Substantiating previous studies9,10, our multimodal cross-species study of the primary motor cortex suggests that a general principle of cortical cell-type organization is its hierarchical relationship, whereby high-level classes linked by major branches comprise progressively finer subpopulations connected by minor branches.”
From A multimodal cell census and atlas of the mammalian primary motor cortex (2021) · cites this paper as [10]
In the citing paper
“Comparing human with mouse and non-human primates reveals both conserved and distinct cell type signatures, including species-specific differences in the proportions of cell populations and in gene expression within homologous cell classes and types (Bakken et al., 2020; Hodge et al., 2019; Krienen et al., 2020).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Hodge et al., 2019
In the citing paper
“Evolutionary conservation and divergence provide insight into the gene regulatory programs that were selected for their impact on cognitive function (Bakken et al., 2020; Hodge et al., 2019; Krienen et al., 2020).”
From Single-Cell Sequencing of Brain Cell Transcriptomes and Epigenomes (2021) · cites this paper as Hodge et al., 2019
In the citing paper
“We observed numerous genes with categorical changes in cell-type-specific expression patterns (including NTNG1, IQGAP2 and TRPC3) and, in rare cases, genes that were a specific marker in one cell class in some species but not detected at all in the interneurons of the other species11”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [11]
In the citing paper
“which suggests that the genes that encode these markers stably delineate a core repertoire of neocortical interneuron types in these species11,15,18”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [11]
In the citing paper
“The expansion of this LAMP5+ LHX6+ cell type throughout the neocortex in diverse primates probably explains a recent observation11 that this cell type is much more abundant in the human temporal lobe than in the mouse V1.”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [11]
In the citing paper
“they obtained 45 human interneuron clusters, whereas our marmoset data resolved to 22 clusters”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [11]
In the citing paper
“However, in agreement with other reports11, these types were inconsistently observed across individual animals and regions, likely due to laminar location and low abundance, and were not analysed further.”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [11]
In the citing paper
“Notably, this approach provides the means to evaluate and compare the circuit contributions and function of PV cINs across species, regardless of their genetic accessibility44,45.”
From Viral manipulation of functionally distinct interneurons in mice, non-human primates and humans (2020) · cites this paper as [44]
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BackgroundMethodInfluentialSelf-citationMouse models of COVID-19 recapitulate inflammatory pathways rather than gene expression
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“Given both cross species conservation and diversity can be 57 identified (14, 15), specifically interrogating any given mouse model for how reliably its 58 transcriptomic responses mimic those seen in humans is clearly warranted (16-18).”
BackgroundHigh-fidelity dendritic sodium spike generation in human layer 2/3 neocortical pyramidal neurons
Gooch, H. M., Bluett, T., Perumal, M. B., Vo, H. D., Fletcher, L. N., Papacostas, J., Jeffree, R. L., Wood, M., Colditz, M., McMillen, J., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111500 · Cited by 35
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“We see the same diversity in human cortex, with all 69 neuron types detected by transcription sequencing in a sample of human neurons matching known types in mice [55].”
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TCF7L2 lncRNA: a link between bipolar disorder and body mass index through glucocorticoid signaling
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“Along a similar vein, divergence of neuro-transmitter receptors and ion channels is known between mouse and human brains 68 .”
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“N-numbers for the first three protocols are stated in d–f, for the other three experiments N-numbers are as follows in chronological order; fITI-DR: Gi (13), Gq (7), Gs (9), Ctrl (20); repeated 9s-fITI: Gi (12), Gq (7), Gs (10), Ctrl (18); vITI: Gi (8 for 1mg/kg, 6 for 10mg/kg), Gq (8), Gs (4), Ctrl (15).”
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“S3) (39–42).”
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The evidence for and consequences of metabotropic glutamate receptor heterodimerization
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Neurotransmitter signaling regulates distinct phases of multimodal human interneuron migration
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“Thus, the characterization of intrinsic migration dynamics has been largely incomplete since defects in migration behavior were inferred from indirect analyses of postmortem mouse and human cortices (Batista-Brito et al , 2008; Chen et al , 2017; Mayer et al , 2018; Hodge et al , 2019).”
Advances in Modeling Alzheimer's Disease In Vitro
Sharma, N. S., Karan, A., Lee, D.-H., Yan, Z., & Xie, J. (2021) · Advanced NanoBiomed Research · doi:10.1002/anbr.202100097 · Cited by 31
The landscape of regulatory genes in brain-wide neuronal phenotypes of a vertebrate brain
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Nogueira, G. O., Garcez, P. P., Bardy, C., Cunningham, M. O., & Sebollela, A. S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.838594 · Cited by 30
Intersectional mapping of multi-transmitter neurons and other cell types in the brain
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“While recent advances in single-cell analysis (Cowan et al., 2020; Hodge et al., 2019; Kim et al., 2020; Peng et al., 2019; Tasic et al., 2016, 2018; Yao et al., 2021; Yuste et al., 2020) provide gene expression patterns that can be used for neuron type enumeration and selective targeting, using…”
Self-citationShwab, E. K., Gingerich, D. C., Man, Z., Gamache, J., Garrett, M. E., Crawford, G. E., Ashley‐Koch, A. E., Serrano, G. E., Beach, T. G., Lutz, M. W., et al. (2024) · Acta Neuropathologica Communications · doi:10.1186/s40478-024-01803-1 · Cited by 25
“Exc1 was the only cluster showing a similar expression profile to Exc5 with relatively high co-expression of three out of the four markers, LAMP5, HPCAL1 and LINC00507 , whereas LINC01500 , an upper cortical layer marker [47], was specifically expressed only in Exc5.”
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Wuyts, F. L., Deblieck, C., Vandevoorde, C., & Durante, M. (2025) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-00923-4 · Cited by 33
“Although cross-species comparisons are essential for functional insights 3 , they should be interpreted with caution because, despite structural similarities, rodents and humans differ in their cellular foundations and transcriptomes 270 .”
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Self-citationThe differential effects of isoflurane and sevoflurane on neonatal mice
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BackgroundModelling the central nervous system: tissue engineering of the cellular microenvironment
Walczak, P. A., Esteban, P. P., Bassett, D. C., & Hill, E. J. (2021) · Emerging Topics in Life Sciences · doi:10.1042/etls20210245 · Cited by 26
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A matter of space and time: Emerging roles of disease-associated proteins in neural development
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Human-Induced Pluripotent Stem Cell Technology: Toward the Future of Personalized Psychiatry
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Metadata
- Authors
- Hodge, R. D., Bakken, T. E., Miller, J. A., Smith, K. A., Barkan, E. R., Graybuck, L. T., Close, J. L., Long, B., Johansen, N., Penn, O., Yao, Z., Eggermont, J., Höllt, T., Levi, B. P., Shehata, S. I., Aevermann, B., Beller, A., Bertagnolli, D., Brouner, K., Casper, T., Cobbs, C., Dalley, R., Dee, N., Ding, S.-L., Ellenbogen, R. G., Fong, O., Garren, E., Goldy, J., Gwinn, R. P., Hirschstein, D., Keene, C. D., Keshk, M., Ko, A. L., Lathia, K., Mahfouz, A., Maltzer, Z., McGraw, M., Nguyen, T. N., Nyhus, J., Ojemann, J. G., Oldre, A., Parry, S., Reynolds, S., Rimorin, C., Shapovalova, N. V., Somasundaram, S., Szafer, A., Thomsen, E. R., Tieu, M., Quon, G., Scheuermann, R. H., Yuste, R., Sunkin, S. M., Lelieveldt, B., Feng, D., Ng, L., Bernard, A., Hawrylycz, M., Phillips, J. W., Tasic, B., Zeng, H., Jones, A. R., Koch, C., & Lein, E. S.
- Affiliations
- Allen Institute for Brain Science (US)
- University of California, Davis (US)
- Leiden University Medical Center (NL)
- J. Craig Venter Institute (US)
- University of Washington (US)
- Swedish Medical Center (US)
- Columbia University (US)
- Corresponding author
- Lein, Ed S.
- ORCID
- Hodge, Rebecca D.
- Bakken, Trygve E.
- Miller, Jeremy A.
- Smith, Kimberly A.
- Barkan, Eliza R.
- Graybuck, Lucas T.
- Close, Jennie L.
- Long, Brian
- Johansen, Nelson
- Yao, Zizhen
- Eggermont, Jeroen
- Höllt, Thomas
- Levi, Boaz P.
- Shehata, Soraya I.
- Aevermann, Brian
- Beller, Allison
- Bertagnolli, Darren
- Brouner, Krissy
- Casper, Tamara
- Cobbs, Charles
- Dalley, Rachel
- Dee, Nick
- Ding, Song-Lin
- Ellenbogen, Richard G.
- Fong, Olivia
- Goldy, Jeff
- Gwinn, Ryder P.
- Hirschstein, Daniel
- Keene, C. Dirk
- Ko, Andrew L.
- Lathia, Kanan
- Mahfouz, Ahmed
- Maltzer, Zoe
- Nguyen, Thuc Nghi
- Nyhus, Julie
- Ojemann, Jeffrey G.
- Oldre, Aaron
- Rimorin, Christine
- Shapovalova, Nadiya V.
- Somasundaram, Saroja
- Szafer, Aaron
- Thomsen, Elliot R.
- Tieu, Michael
- Quon, Gerald
- Scheuermann, Richard H.
- Yuste, Rafael
- Sunkin, Susan M.
- Lelieveldt, Boudewijn
- Feng, David
- Ng, Lydia
- Bernard, Amy
- Hawrylycz, Michael
- Phillips, John W.
- Tasic, Bosiljka
- Zeng, Hongkui
- Lein, Ed S.
- Venue
- Nature
- Published
- 2019-08-21
- Volume
- 573
- Issue
- 7772
- Pages
- 61-68
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6919571
- OpenAlex
- W2969948459
- Cited by
- 1,775
- References
- 89
- Citations by year
- 2026: 199 · 2025: 242 · 2024: 275 · 2023: 269 · 2022: 235 · 2021: 289 · 2020: 212 · 2019: 43
- FWCI
- 64.09
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- University of Washington
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (12720, 12721)
- National Institutes of Health (5u01mh114812-03, MH114812-02)
- National Institute of Mental Health (U01MH105982, U01MH114812, U19MH114830)
- National Institute of General Medical Sciences (T32GM008497)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- human cerebral cortex, middle temporal gyrus, cortical cell types, excitatory neurons, inhibitory neurons, single-nucleus RNA sequencing, human-mouse comparison, cortical laminar organization, species differences, neuronal morphology, gene expression
- MeSH terms
- RNA-Seq, Adolescent, Adult, Aged, Animals, Astrocytes, Cerebral Cortex, Biological Evolution, Female, Humans, Male, Middle Aged, Neural Inhibition, Neurons, Species Specificity, Principal Component Analysis, Mice, Young Adult, Single-Cell Analysis, Transcriptome
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