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Morphoelectric and transcriptomic divergence of the layer 1 interneuron repertoire in human versus mouse neocortex

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Chartrand, Thomas, Dalley, Rachel, Close, Jennie, Goriounova, Natalia A., Lee, Brian R., Mann, Rusty, Miller, Jeremy A., Molnar, Gabor +82 more·2023·Science
DOI 10.1126/science.adf0805PMC PMC11864503

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Abstract

Neocortical layer 1 (L1) is a site of convergence between pyramidal-neuron dendrites and feedback axons where local inhibitory signaling can profoundly shape cortical processing. Evolutionary expansion of human neocortex is marked by distinctive pyramidal neurons with extensive L1 branching, but whether L1 interneurons are similarly diverse is underexplored. Using Patch-seq recordings from human neurosurgical tissue, we identified four transcriptomic subclasses with mouse L1 homologs, along with distinct subtypes and types unmatched in mouse L1. Subclass and subtype comparisons showed stronger transcriptomic differences in human L1 and were correlated with strong morphoelectric variability along dimensions distinct from mouse L1 variability. Accompanied by greater layer thickness and other cytoarchitecture changes, these findings suggest that L1 has diverged in evolution, reflecting the demands of regulating the expanded human neocortical circuit.

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  • BICCN and BICAN reference classifications provide a foundational reference to understand the cellular, molecular and epigenomic underpinnings of AD.

    “These reference classifications provide an extremely powerful foundational reference to understand the cellular, molecular and epigenomic underpinnings of AD.”

    From Integrated multimodal cell atlas of Alzheimer’s disease (2024) · cites this paper as [22]

    The Discussion (‘Categorizing L1 neuron types’; page unavailable) describes classifications of human and mouse layer 1 interneurons, supporting the claim that this work provides a cellular reference. It does not say that BICCN or BICAN classifications provide a foundation for understanding Alzheimer’s disease (AD) or its epigenomic underpinnings. A paper on Alzheimer’s disease appears in the References, but that listing does not establish the claimed application. (LLM, conf=0.82)

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  • The typical morphoelectrical properties of MGE supertypes were recently characterized using patch-seq profiling in neurosurgically resected tissues from human donors without AD, and the supragranular localization of vulnerable Sst and Pvalb interneurons was qualitatively confirmed.

    “The typical morphoelectrical properties (that is, before disease onset) of the MGE supertypes were recently characterized using patch-seq profiling in neurosurgically resected tissues from human donors without AD21,22; the supragranular localization of vulnerable Sst and Pvalb interneurons was qualitatively confirmed.”

    From Integrated multimodal cell atlas of Alzheimer’s disease (2024) · cites this paper as [22]

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  • Integrated multimodal cell atlas of Alzheimer’s disease

    Gabitto, M. I., Travaglini, K. J., Rachleff, V. M., Kaplan, E. S., Long, B., Ariza, J., Ding, Y., Mahoney, J. T., Dee, N., Goldy, J., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01774-5 · Cited by 397 · see citing works

    “…Initiative Cell Atlas Network (BICAN) has established best practices in experimental and quantitative analyses to harness single-cell genomics, spatial transcriptomics and patch sequencing (patch-seq) methods to characterize cellular properties and build a knowledge base of brain cell types 16–22 .”
    InfluentialSelf-citation

Authors
Chartrand, T., Dalley, R., Close, J., Goriounova, N. A., Lee, B. R., Mann, R., Miller, J. A., Molnar, G., Mukora, A., Alfiler, L., Baker, K., Bakken, T. E., Berg, J., Bertagnolli, D., Braun, T., Brouner, K., Casper, T., Csajbok, E. A., Dee, N., Egdorf, T., Enstrom, R., Galakhova, A. A., Gary, A., Gelfand, E., Goldy, J., Hadley, K., Heistek, T. S., Hill, D., Jorstad, N., Kim, L., Kocsis, A. K., Kruse, L., Kunst, M., Leon, G., Long, B., Mallory, M., McGraw, M., McMillen, D., Melief, E. J., Mihut, N., Ng, L., Nyhus, J., Oláh, G., Ozsvár, A., Omstead, V., Peterfi, Z., Pom, A., Potekhina, L., Rajanbabu, R., Rozsa, M., Ruiz, A., Sandle, J., Sunkin, S. M., Szots, I., Tieu, M., Toth, M., Trinh, J., Vargas, S., Vumbaco, D., Williams, G., Wilson, J., Yao, Z., Barzo, P., Cobbs, C., Ellenbogen, R. G., Esposito, L., Ferreira, M., Gouwens, N. W., Grannan, B., Gwinn, R. P., Hauptman, J. S., Jarsky, T., Keene, C. D., Ko, A. L., Koch, C., Ojemann, J. G., Patel, A., Ruzevick, J., Silbergeld, D. L., Smith, K., Sorensen, S. A., Tasic, B., Ting, J. T., Waters, J., de Kock, C. P. J., Mansvelder, H. D., Tamas, G., Zeng, H., Kalmbach, B., & Lein, E. S.
Affiliations
  • Allen Institute for Brain Science (US)
  • Vrije Universiteit Amsterdam (NL)
  • Research Group for Cortical Microcircuits of the Hungarian Academy of Science, University of Szeged, Szeged, Hungary.
  • byte physics, Berlin, Germany.
  • Allen Institute for Brain Science, Seattle, WA, USA.
  • University of Szeged (HU)
  • University of Washington (US)
  • Department of Neurosurgery, University of Szeged, Szeged, Hungary.
  • Swedish Medical Center (US)
  • Center for Neurogenomics and Cognitive Research, Vrije Universiteit, Amsterdam, Netherlands.
Corresponding author
  • Chartrand, Thomas
  • Kalmbach, Brian
  • Lein, Ed S.
ORCID
Venue
Science
Publisher
American Association for the Advancement of Science (AAAS)
Published
2023-10-13
Volume
382
Issue
6667
Pages
eadf0805-eadf0805
ISSN
  • 0036-8075 (ISSN-L)
  • 1095-9203
DOI
10.1126/science.adf0805
PMC
PMC11864503
OpenAlex
W4387595301
Cited by
88
References
27
Citations by year
2026: 19 · 2025: 29 · 2024: 32 · 2023: 7 · 2022: 1
FWCI
10.55
Type
journal article
Language
en
Open access
Licence
cc-by-nd
Locations
  • Science (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • SZTE Publicatio Repozitórium (University of Szeged) (submittedVersion)
  • VU Research Portal (submittedVersion, other-oa)
Funders
  • Nancy and Buster Alvord Endowment
  • European Commission (ÚNKP-20-5, 20391-3/2018/FEKUSTRAT, ÚNKP-21-5, HORIZON2020, 945539)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (024.004.012, OCENW.M20.285, VI.Vidi.213.014, OCENW.M20)
  • Magyar Tudományos Akadémia (20391-3/2018/FEKUSTRAT, NKP-20-5, ÚNKP-21-5)
  • Emberi Eroforrások Minisztériuma (ÚNKP-21-5, 20391‐3/2018/FEKUSTRAT, 20391-3/2018)
  • Innovációs és Technológiai Minisztérium (TKP2021-EGA-28, ÚNKP-21-5-SZTE-580, ÚNKP-20-5, TKP2021, NKP-21-5)
  • Szegedi Tudományegyetem (20391-3/2018/FEKUSTRAT)
  • National Institutes of Health (5u01mh114812-03, 1rf1mh128778-01, 945539, 20391-3, U01MH114812)
  • Horizon 2020 Framework Programme (#945539)
  • Nemzeti Kutatási, Fejlesztési és Innovaciós Alap (ÚNKP-21-5, 2019-2.1.7-ERA-NET, TKP2021-EGA, TKP2021-EGA-28, TKP2021, ÚNKP‐20‐5, ÚNKP-20, 20391-3/2018/FEKUSTRAT)
  • National Research, Development and Innovation Office (20391-3/2018/FEKUSTRAT, TKP2021-EGA-28, TKP-2021-EGA, TKP2021-EGA09, ÚNKP-21-5, ÚNKP-20-5, TKP 2021)
  • National Institute of Mental Health (945539, R01MH116247, U01MH114812, RF1 MH128778)
  • HORIZON EUROPE European Research Council (101093198)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
Keywords
interneurons, human-mouse divergence, Patch-seq, cortical inhibition, pyramidal neurons, layer thickness, cytoarchitecture, cortical circuits
MeSH terms
Animals, Axons, Humans, Interneurons, Pyramidal Cells, Neocortex, Mice, Transcriptome

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