Human neocortical expansion involves glutamatergic neuron diversification

Berg, Jim; Sorensen, Staci A.; Ting, Jonathan T.; Miller, Jeremy A.; Chartrand, Thomas; Buchin, Anatoly; Bakken, Trygve E.; Budzillo, Agata; Dee, Nick; Ding, Song-Lin; Gouwens, Nathan W.; Hodge, Rebecca D.; Kalmbach, Brian; Lee, Changkyu; Lee, Brian R.; Alfiler, Lauren; Baker, Katherine; Barkan, Eliza; Beller, Allison; Berry, Kyla; Bertagnolli, Darren; Bickley, Kris; Bomben, Jasmine; Braun, Thomas; Brouner, Krissy; Casper, Tamara; Chong, Peter; Crichton, Kirsten; Dalley, Rachel; Frates, Rebecca; Desta, Tsega; Lee, Samuel Dingman; D’Orazi, Florence; Dotson, Nadezhda; Egdorf, Tom; Enstrom, Rachel; Farrell, Colin; Feng, David; Fong, Olivia; Furdan, Szabina; Galakhova, Anna A.; Gamlin, Clare; Gary, Amanda; Glandon, Alexandra; Goldy, Jeff; Gorham, Melissa; Goriounova, Natalia A.; Gratiy, Sergey; Graybuck, Lucas; Gu, Hong; Hadley, Kristen; Hansen, Nathan; Heistek, Tim S.; Henry, Alex M.; Heyer, Djai B.; Hill, DiJon; Hill, Chris; Hupp, Madie; Jarsky, Tim; Kebede, Sara; Keene, Lisa; Kim, Lisa; Kim, Mean-Hwan; Kroll, Matthew; Latimer, Caitlin; Levi, Boaz P.; Link, Katherine E.; Mallory, Matthew; Mann, Rusty; Marshall, Desiree; Maxwell, Michelle; McGraw, Medea; McMillen, Delissa; Melief, Erica; Mertens, Eline J.; Mezei, Leona; Mihut, Norbert; Mok, Stephanie; Molnar, Gabor; Mukora, Alice; Ng, Lindsay; Ngo, Kiet; Nicovich, Philip R.; Nyhus, Julie; Olah, Gaspar; Oldre, Aaron; Omstead, Victoria; Ozsvar, Attila; Park, Daniel; Peng, Hanchuan; Pham, Trangthanh; Pom, Christina A.; Potekhina, Lydia; Rajanbabu, Ramkumar; Ransford, Shea; Reid, David; Rimorin, Christine; Ruiz, Augustin; Sandman, David; Sulc, Josef; Sunkin, Susan M.; Szafer, Aaron; Szemenyei, Viktor; Thomsen, Elliot R.; Tieu, Michael; Torkelson, Amy; Trinh, Jessica; Tung, Herman; Wakeman, Wayne; Waleboer, Femke; Ward, Katelyn; Wilbers, René; Williams, Grace; Yao, Zizhen; Yoon, Jae-Geun; Anastassiou, Costas; Arkhipov, Anton; Barzo, Pal; Bernard, Amy; Cobbs, Charles; Hamer, Philip C. Witt; Ellenbogen, Richard G.; Esposito, Luke; Ferreira, Manuel; Gwinn, Ryder P.; Hawrylycz, Michael J.; Hof, Patrick R.; Idema, Sander; Jones, Allan R.; Keene, C. Dirk; Ko, Andrew L.; Murphy, Gabe J.; Ng, Lydia; Ojemann, Jeffrey G.; Patel, Anoop P.; Phillips, John W.; Silbergeld, Daniel L.; Smith, Kimberly; Tasic, Bosiljka; Yuste, Rafael; Segev, Idan; Kock, Christiaan P. J.; Mansvelder, Huibert D.; Tamas, Gabor; Zeng, Hongkui; Koch, Christof; Lein, Ed S.

Human neocortical expansion involves glutamatergic neuron diversification

Jim Berg, Staci A. Sorensen, Jonathan T. Ting, Jeremy A. Miller, Thomas Chartrand, Anatoly Buchin, Trygve E. Bakken, Agata Budzillo, Nick Dee, Song-Lin Ding, Nathan W. Gouwens, Rebecca D. Hodge, Brian Kalmbach, Changkyu Lee, Brian R. Lee, Lauren Alfiler, Katherine Baker, Eliza Barkan, Allison Beller, Kyla Berry, Darren Bertagnolli, Kris Bickley, Jasmine Bomben, Thomas Braun, Krissy Brouner, Tamara Casper, Peter Chong, Kirsten Crichton, Rachel Dalley, Rebecca Frates, Tsega Desta, Samuel Dingman Lee, Florence D’Orazi, Nadezhda Dotson, Tom Egdorf, Rachel Enstrom, Colin Farrell, David Feng, Olivia Fong, Szabina Furdan, Anna A. Galakhova, Clare Gamlin, Amanda Gary, Alexandra Glandon, Jeff Goldy, Melissa Gorham, Natalia A. Goriounova, Sergey Gratiy, Lucas Graybuck, Hong Gu, Kristen Hadley, Nathan Hansen, Tim S. Heistek, Alex M. Henry, Djai B. Heyer, DiJon Hill, Chris Hill, Madie Hupp, Tim Jarsky, Sara Kebede, Lisa Keene, Lisa Kim, Mean-Hwan Kim, Matthew Kroll, Caitlin Latimer, Boaz P. Levi, Katherine E. Link, Matthew Mallory, Rusty Mann, Desiree Marshall, Michelle Maxwell, Medea McGraw, Delissa McMillen, Erica Melief, Eline J. Mertens, Leona Mezei, Norbert Mihut, Stephanie Mok, Gabor Molnar, Alice Mukora, Lindsay Ng, Kiet Ngo, Philip R. Nicovich, Julie Nyhus, Gaspar Olah, Aaron Oldre, Victoria Omstead, Attila Ozsvar, Daniel Park, Hanchuan Peng, Trangthanh Pham, Christina A. Pom, Lydia Potekhina, Ramkumar Rajanbabu, Shea Ransford, David Reid, Christine Rimorin, Augustin Ruiz, David Sandman, Josef Sulc, Susan M. Sunkin, Aaron Szafer, Viktor Szemenyei, Elliot R. Thomsen, Michael Tieu, Amy Torkelson, Jessica Trinh, Herman Tung, Wayne Wakeman, Femke Waleboer, Katelyn Ward, René Wilbers, Grace Williams, Zizhen Yao, Jae-Geun Yoon, Costas Anastassiou, Anton Arkhipov, Pal Barzo, Amy Bernard, Charles Cobbs, Philip C. Witt Hamer, Richard G. Ellenbogen, Luke Esposito, Manuel Ferreira, Ryder P. Gwinn, Michael J. Hawrylycz, Patrick R. Hof, Sander Idema, Allan R. Jones, C. Dirk Keene, Andrew L. Ko, Gabe J. Murphy, Lydia Ng, Jeffrey G. Ojemann, Anoop P. Patel, John W. Phillips, Daniel L. Silbergeld, Kimberly Smith, Bosiljka Tasic, Rafael Yuste, Idan Segev, Christiaan P. J. Kock, Huibert D. Mansvelder, Gabor Tamas, Hongkui Zeng, Christof Koch and Ed S. Lein ()
Additional contact information
Jim Berg: Allen Institute for Brain Science
Staci A. Sorensen: Allen Institute for Brain Science
Jonathan T. Ting: Allen Institute for Brain Science
Jeremy A. Miller: Allen Institute for Brain Science
Thomas Chartrand: Allen Institute for Brain Science
Anatoly Buchin: Allen Institute for Brain Science
Trygve E. Bakken: Allen Institute for Brain Science
Agata Budzillo: Allen Institute for Brain Science
Nick Dee: Allen Institute for Brain Science
Song-Lin Ding: Allen Institute for Brain Science
Nathan W. Gouwens: Allen Institute for Brain Science
Rebecca D. Hodge: Allen Institute for Brain Science
Brian Kalmbach: Allen Institute for Brain Science
Changkyu Lee: Allen Institute for Brain Science
Brian R. Lee: Allen Institute for Brain Science
Lauren Alfiler: Allen Institute for Brain Science
Katherine Baker: Allen Institute for Brain Science
Eliza Barkan: Allen Institute for Brain Science
Allison Beller: University of Washington
Kyla Berry: Allen Institute for Brain Science
Darren Bertagnolli: Allen Institute for Brain Science
Kris Bickley: Allen Institute for Brain Science
Jasmine Bomben: Allen Institute for Brain Science
Thomas Braun: byte physics
Krissy Brouner: Allen Institute for Brain Science
Tamara Casper: Allen Institute for Brain Science
Peter Chong: Allen Institute for Brain Science
Kirsten Crichton: Allen Institute for Brain Science
Rachel Dalley: Allen Institute for Brain Science
Rebecca Frates: Allen Institute for Brain Science
Tsega Desta: Allen Institute for Brain Science
Samuel Dingman Lee: Allen Institute for Brain Science
Florence D’Orazi: Allen Institute for Brain Science
Nadezhda Dotson: Allen Institute for Brain Science
Tom Egdorf: Allen Institute for Brain Science
Rachel Enstrom: Allen Institute for Brain Science
Colin Farrell: Allen Institute for Brain Science
David Feng: Allen Institute for Brain Science
Olivia Fong: Allen Institute for Brain Science
Szabina Furdan: University of Szeged
Anna A. Galakhova: Vrije Universiteit
Clare Gamlin: Allen Institute for Brain Science
Amanda Gary: Allen Institute for Brain Science
Alexandra Glandon: Allen Institute for Brain Science
Jeff Goldy: Allen Institute for Brain Science
Melissa Gorham: Allen Institute for Brain Science
Natalia A. Goriounova: Vrije Universiteit
Sergey Gratiy: Allen Institute for Brain Science
Lucas Graybuck: Allen Institute for Brain Science
Hong Gu: Allen Institute for Brain Science
Kristen Hadley: Allen Institute for Brain Science
Nathan Hansen: Swedish Neuroscience Institute
Tim S. Heistek: Vrije Universiteit
Alex M. Henry: Allen Institute for Brain Science
Djai B. Heyer: Vrije Universiteit
DiJon Hill: Allen Institute for Brain Science
Chris Hill: Allen Institute for Brain Science
Madie Hupp: Allen Institute for Brain Science
Tim Jarsky: Allen Institute for Brain Science
Sara Kebede: Allen Institute for Brain Science
Lisa Keene: University of Washington
Lisa Kim: Allen Institute for Brain Science
Mean-Hwan Kim: Allen Institute for Brain Science
Matthew Kroll: Allen Institute for Brain Science
Caitlin Latimer: University of Washington
Boaz P. Levi: Allen Institute for Brain Science
Katherine E. Link: Allen Institute for Brain Science
Matthew Mallory: Allen Institute for Brain Science
Rusty Mann: Allen Institute for Brain Science
Desiree Marshall: University of Washington
Michelle Maxwell: Allen Institute for Brain Science
Medea McGraw: Allen Institute for Brain Science
Delissa McMillen: Allen Institute for Brain Science
Erica Melief: University of Washington
Eline J. Mertens: Vrije Universiteit
Leona Mezei: University of Szeged
Norbert Mihut: University of Szeged
Stephanie Mok: Allen Institute for Brain Science
Gabor Molnar: University of Szeged
Alice Mukora: Allen Institute for Brain Science
Lindsay Ng: Allen Institute for Brain Science
Kiet Ngo: Allen Institute for Brain Science
Philip R. Nicovich: Allen Institute for Brain Science
Julie Nyhus: Allen Institute for Brain Science
Gaspar Olah: University of Szeged
Aaron Oldre: Allen Institute for Brain Science
Victoria Omstead: Allen Institute for Brain Science
Attila Ozsvar: University of Szeged
Daniel Park: Allen Institute for Brain Science
Hanchuan Peng: Allen Institute for Brain Science
Trangthanh Pham: Allen Institute for Brain Science
Christina A. Pom: Allen Institute for Brain Science
Lydia Potekhina: Allen Institute for Brain Science
Ramkumar Rajanbabu: Allen Institute for Brain Science
Shea Ransford: Allen Institute for Brain Science
David Reid: Allen Institute for Brain Science
Christine Rimorin: Allen Institute for Brain Science
Augustin Ruiz: Allen Institute for Brain Science
David Sandman: Allen Institute for Brain Science
Josef Sulc: Allen Institute for Brain Science
Susan M. Sunkin: Allen Institute for Brain Science
Aaron Szafer: Allen Institute for Brain Science
Viktor Szemenyei: University of Szeged
Elliot R. Thomsen: Allen Institute for Brain Science
Michael Tieu: Allen Institute for Brain Science
Amy Torkelson: Allen Institute for Brain Science
Jessica Trinh: Allen Institute for Brain Science
Herman Tung: Allen Institute for Brain Science
Wayne Wakeman: Allen Institute for Brain Science
Femke Waleboer: Vrije Universiteit
Katelyn Ward: Allen Institute for Brain Science
René Wilbers: Vrije Universiteit
Grace Williams: Allen Institute for Brain Science
Zizhen Yao: Allen Institute for Brain Science
Jae-Geun Yoon: Swedish Neuroscience Institute
Costas Anastassiou: Allen Institute for Brain Science
Anton Arkhipov: Allen Institute for Brain Science
Pal Barzo: University of Szeged
Amy Bernard: Allen Institute for Brain Science
Charles Cobbs: Swedish Neuroscience Institute
Philip C. Witt Hamer: Vrije Universiteit
Richard G. Ellenbogen: University of Washington
Luke Esposito: Allen Institute for Brain Science
Manuel Ferreira: University of Washington
Ryder P. Gwinn: Swedish Neuroscience Institute
Michael J. Hawrylycz: Allen Institute for Brain Science
Patrick R. Hof: Icahn School of Medicine at Mount Sinai
Sander Idema: Vrije Universiteit
Allan R. Jones: Allen Institute for Brain Science
C. Dirk Keene: University of Washington
Andrew L. Ko: University of Washington
Gabe J. Murphy: Allen Institute for Brain Science
Lydia Ng: Allen Institute for Brain Science
Jeffrey G. Ojemann: University of Washington
Anoop P. Patel: University of Washington
John W. Phillips: Allen Institute for Brain Science
Daniel L. Silbergeld: University of Washington
Kimberly Smith: Allen Institute for Brain Science
Bosiljka Tasic: Allen Institute for Brain Science
Rafael Yuste: Columbia University
Idan Segev: The Hebrew University Jerusalem
Christiaan P. J. Kock: Vrije Universiteit
Huibert D. Mansvelder: Vrije Universiteit
Gabor Tamas: University of Szeged
Hongkui Zeng: Allen Institute for Brain Science
Christof Koch: Allen Institute for Brain Science
Ed S. Lein: Allen Institute for Brain Science

Nature, 2021, vol. 598, issue 7879, 151-158

Abstract: Abstract The neocortex is disproportionately expanded in human compared with mouse1,2, both in its total volume relative to subcortical structures and in the proportion occupied by supragranular layers composed of neurons that selectively make connections within the neocortex and with other telencephalic structures. Single-cell transcriptomic analyses of human and mouse neocortex show an increased diversity of glutamatergic neuron types in supragranular layers in human neocortex and pronounced gradients as a function of cortical depth3. Here, to probe the functional and anatomical correlates of this transcriptomic diversity, we developed a robust platform combining patch clamp recording, biocytin staining and single-cell RNA-sequencing (Patch-seq) to examine neurosurgically resected human tissues. We demonstrate a strong correspondence between morphological, physiological and transcriptomic phenotypes of five human glutamatergic supragranular neuron types. These were enriched in but not restricted to layers, with one type varying continuously in all phenotypes across layers 2 and 3. The deep portion of layer 3 contained highly distinctive cell types, two of which express a neurofilament protein that labels long-range projection neurons in primates that are selectively depleted in Alzheimer’s disease4,5. Together, these results demonstrate the explanatory power of transcriptomic cell-type classification, provide a structural underpinning for increased complexity of cortical function in humans, and implicate discrete transcriptomic neuron types as selectively vulnerable in disease.

Date: 2021
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DOI: 10.1038/s41586-021-03813-8

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