Signature morphoelectric properties of diverse GABAergic interneurons in the human neocortex

Author:

Lee Brian R.1ORCID,Dalley Rachel1ORCID,Miller Jeremy A.1ORCID,Chartrand Thomas12ORCID,Close Jennie1ORCID,Mann Rusty1ORCID,Mukora Alice1ORCID,Ng Lindsay1ORCID,Alfiler Lauren1ORCID,Baker Katherine1ORCID,Bertagnolli Darren1ORCID,Brouner Krissy1ORCID,Casper Tamara1ORCID,Csajbok Eva3ORCID,Donadio Nicholas1ORCID,Driessens Stan L.W.4,Egdorf Tom1ORCID,Enstrom Rachel1ORCID,Galakhova Anna A.4ORCID,Gary Amanda1ORCID,Gelfand Emily1ORCID,Goldy Jeff1ORCID,Hadley Kristen1ORCID,Heistek Tim S.4,Hill Dijon1ORCID,Hou Wen-Hsien5,Johansen Nelson1ORCID,Jorstad Nik1ORCID,Kim Lisa12ORCID,Kocsis Agnes Katalin3ORCID,Kruse Lauren1ORCID,Kunst Michael1ORCID,León Gabriela1,Long Brian1ORCID,Mallory Matthew1ORCID,Maxwell Michelle1,McGraw Medea1ORCID,McMillen Delissa1ORCID,Melief Erica J.6ORCID,Molnar Gabor3ORCID,Mortrud Marty T.1,Newman Dakota1,Nyhus Julie1ORCID,Opitz-Araya Ximena1ORCID,Ozsvár Attila5,Pham Trangthanh1ORCID,Pom Alice1ORCID,Potekhina Lydia1ORCID,Rajanbabu Ram1ORCID,Ruiz Augustin1ORCID,Sunkin Susan M.1ORCID,Szöts Ildikó3ORCID,Taskin Naz1,Thyagarajan Bargavi1ORCID,Tieu Michael1ORCID,Trinh Jessica1ORCID,Vargas Sara1,Vumbaco David1ORCID,Waleboer Femke4ORCID,Walling-Bell Sarah1ORCID,Weed Natalie1ORCID,Williams Grace1ORCID,Wilson Julia1,Yao Shenqin1ORCID,Zhou Thomas1ORCID,Barzó Pál7ORCID,Bakken Trygve1ORCID,Cobbs Charles8ORCID,Dee Nick1ORCID,Ellenbogen Richard G.9ORCID,Esposito Luke1ORCID,Ferreira Manuel9,Gouwens Nathan W.1,Grannan Benjamin9ORCID,Gwinn Ryder P.8ORCID,Hauptman Jason S.9,Hodge Rebecca1ORCID,Jarsky Tim1ORCID,Keene C. Dirk6ORCID,Ko Andrew L.9ORCID,Korshoej Anders Rosendal10ORCID,Levi Boaz P.1ORCID,Meier Kaare1011ORCID,Ojemann Jeffrey G.9ORCID,Patel Anoop9,Ruzevick Jacob9,Silbergeld Daniel L.9,Smith Kimberly1ORCID,Sørensen Jens Christian1012ORCID,Waters Jack113ORCID,Zeng Hongkui1ORCID,Berg Jim12ORCID,Capogna Marco5ORCID,Goriounova Natalia A.4ORCID,Kalmbach Brian113ORCID,de Kock Christiaan P.J.4ORCID,Mansvelder Huib D.4ORCID,Sorensen Staci A.1,Tamas Gabor3ORCID,Lein Ed S.19ORCID,Ting Jonathan T.113ORCID

Affiliation:

1. Allen Institute for Brain Science, Seattle, WA 98109, USA.

2. Allen Institute for Neural Dynamics, Seattle, WA 98109, USA.

3. MTA-SZTE Research Group for Cortical Microcircuits, Department of Physiology, Anatomy, and Neuroscience, University of Szeged, 6726 Szeged, Hungary.

4. Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit, Amsterdam, 1081 HV, Netherlands.

5. Department of Biomedicine, Aarhus University, 8000 Aarhus, Denmark.

6. Department of Laboratory Medicine and Pathology, University of Washington, Seattle, WA 98195, USA.

7. Department of Neurosurgery, University of Szeged, 6725 Szeged, Hungary.

8. Swedish Neuroscience Institute, Seattle, WA 98122, USA.

9. Department of Neurological Surgery, University of Washington, Seattle, WA 98195, USA.

10. Department of Neurosurgery, Aarhus University Hospital, 8200 Aarhus, Denmark.

11. Department of Anesthesiology, Aarhus University Hospital, 8200 Aarhus, Denmark.

12. Center for Experimental Neuroscience, Aarhus University Hospital, 8200 Aarhus, Denmark.

13. Department of Physiology and Biophysics, University of Washington, Seattle, WA 98195, USA.

Abstract

Human cortex transcriptomic studies have revealed a hierarchical organization of γ-aminobutyric acid–producing (GABAergic) neurons from subclasses to a high diversity of more granular types. Rapid GABAergic neuron viral genetic labeling plus Patch-seq (patch-clamp electrophysiology plus single-cell RNA sequencing) sampling in human brain slices was used to reliably target and analyze GABAergic neuron subclasses and individual transcriptomic types. This characterization elucidated transitions between PVALB and SST subclasses, revealed morphological heterogeneity within an abundant transcriptomic type, identified multiple spatially distinct types of the primate-specialized double bouquet cells (DBCs), and shed light on cellular differences between homologous mouse and human neocortical GABAergic neuron types. These results highlight the importance of multimodal phenotypic characterization for refinement of emerging transcriptomic cell type taxonomies and for understanding conserved and specialized cellular properties of human brain cell types.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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