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1. Human neocortical expansion involves glutamatergic neuron diversification

Author

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

Subjects
Cell type, Multidisciplinary, Neocortex, Neurofilament, Molecular neuroscience, Biology, Article, Cellular neuroscience, chemistry.chemical_compound, Glutamatergic, medicine.anatomical_structure, chemistry, Biocytin, medicine, Neuron, Neuroscience
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., Combined patch clamp recording, biocytin staining and single-cell RNA-sequencing of human neurocortical neurons shows an expansion of glutamatergic neuron types relative to mouse that characterizes the greater complexity of the human neocortex.

Published
2021

2. Author Correction: Comparative cellular analysis of motor cortex in human, marmoset and mouse

Author

Trygve E. Bakken, Nikolas L. Jorstad, Qiwen Hu, Blue B. Lake, Wei Tian, Brian E. Kalmbach, Megan Crow, Rebecca D. Hodge, Fenna M. Krienen, Staci A. Sorensen, Jeroen Eggermont, Zizhen Yao, Brian D. Aevermann, Andrew I. Aldridge, Anna Bartlett, Darren Bertagnolli, Tamara Casper, Rosa G. Castanon, Kirsten Crichton, Tanya L. Daigle, Rachel Dalley, Nick Dee, Nikolai Dembrow, Dinh Diep, Song-Lin Ding, Weixiu Dong, Rongxin Fang, Stephan Fischer, Melissa Goldman, Jeff Goldy, Lucas T. Graybuck, Brian R. Herb, Xiaomeng Hou, Jayaram Kancherla, Matthew Kroll, Kanan Lathia, Baldur van Lew, Yang Eric Li, Christine S. Liu, Hanqing Liu, Jacinta D. Lucero, Anup Mahurkar, Delissa McMillen, Jeremy A. Miller, Marmar Moussa, Joseph R. Nery, Philip R. Nicovich, Sheng-Yong Niu, Joshua Orvis, Julia K. Osteen, Scott Owen, Carter R. Palmer, Thanh Pham, Nongluk Plongthongkum, Olivier Poirion, Nora M. Reed, Christine Rimorin, Angeline Rivkin, William J. Romanow, Adriana E. Sedeño-Cortés, Kimberly Siletti, Saroja Somasundaram, Josef Sulc, Michael Tieu, Amy Torkelson, Herman Tung, Xinxin Wang, Fangming Xie, Anna Marie Yanny, Renee Zhang, Seth A. Ament, M. Margarita Behrens, Hector Corrada Bravo, Jerold Chun, Alexander Dobin, Jesse Gillis, Ronna Hertzano, Patrick R. Hof, Thomas Höllt, Gregory D. Horwitz, C. Dirk Keene, Peter V. Kharchenko, Andrew L. Ko, Boudewijn P. Lelieveldt, Chongyuan Luo, Eran A. Mukamel, António Pinto-Duarte, Sebastian Preiss, Aviv Regev, Bing Ren, Richard H. Scheuermann, Kimberly Smith, William J. Spain, Owen R. White, Christof Koch, Michael Hawrylycz, Bosiljka Tasic, Evan Z. Macosko, Steven A. McCarroll, Jonathan T. Ting, Hongkui Zeng, Kun Zhang, Guoping Feng, Joseph R. Ecker, Sten Linnarsson, and Ed S. Lein

Subjects
Multidisciplinary
Published
2022

3. A transcriptomic and epigenomic cell atlas of the mouse primary motor cortex

Author

Cindy T. J. van Velthoven, Eran A. Mukamel, Kanan Lathia, Jeff Goldy, Elizabeth Purdom, Hanqing Liu, Zizhen Yao, Xinxin Wang, Victor Felix, Olivia Fong, Brian R. Herb, Jacinta Lucero, Elizabeth L. Dougherty, Carlo Colantuoni, Thanh Pham, Bing Ren, Valentine Svensson, Sheng-Yong Niu, Rongxin Fang, Davide Risso, Seth A. Ament, Michael Tieu, Christine Rimorin, John Ngai, Ricky S. Adkins, Sandrine Dudoit, Naeem Nadaf, Stephan Fischer, Michael Hawrylycz, Evan Z. Macosko, Anup Mahurkar, Joshua Orvis, Lior Pachter, Thuc Nghi Nguyen, Peter V. Kharchenko, Vasilis Ntranos, Bosiljka Tasic, Joshua D. Welch, Darren Bertagnolli, Charles R. Vanderburg, Yang Eric Li, Eeshit Dhaval Vaishnav, Xiaomeng Hou, Joseph R. Ecker, Delissa McMillen, Kirsten Crichton, Heather Huot Creasy, Antonio Pinto-Duarte, Josef Sulc, A. Sina Booeshaghi, Megan Crow, Chongyuan Luo, Owen White, Kimberly A. Smith, Jayaram Kancherla, Jonathan Crabtree, Herman Tung, Wayne I. Doyle, Angeline Rivkin, M. Margarita Behrens, Hongkui Zeng, Kelly Street, Amy Torkelson, Tommaso Biancalani, Julia K. Osteen, Héctor Corrada Bravo, Aviv Regev, Anna Bartlett, Olivier Poirion, Nick Dee, Qiwen Hu, Michelle G. Giglio, Z. Josh Huang, Andrew Aldridge, Ronna Hertzano, Sebastian Preissl, Matthew Kroll, Koen Van den Berge, Fangming Xie, Jesse Gillis, Joseph R. Nery, Tamara Casper, and Hector Roux de Bézieux

Subjects
Epigenomics, Male, Cell type, General Science & Technology, 1.1 Normal biological development and functioning, Population, Datasets as Topic, Bioengineering, Molecular neuroscience, Computational biology, Biology, CLASSIFICATION, Article, Epigenesis, Genetic, Mice, Atlases as Topic, Single-cell analysis, Genetic, Underpinning research, MAPS, medicine, Genetics, Animals, education, Neurons, education.field_of_study, ARCHITECTURE, Multidisciplinary, Gene Expression Profiling, Human Genome, Neurosciences, Motor Cortex, Biology and Life Sciences, Reproducibility of Results, Cellular neuroscience, Gene expression profiling, medicine.anatomical_structure, Mathematics and Statistics, Organ Specificity, Neurological, Female, Primary motor cortex, Single-Cell Analysis, Transcriptome, Motor cortex, Epigenesis, Biotechnology
Abstract

Single-cell transcriptomics can provide quantitative molecular signatures for large, unbiased samples of the diverse cell types in the brain1–3. With the proliferation of multi-omics datasets, a major challenge is to validate and integrate results into a biological understanding of cell-type organization. Here we generated transcriptomes and epigenomes from more than 500,000 individual cells in the mouse primary motor cortex, a structure that has an evolutionarily conserved role in locomotion. We developed computational and statistical methods to integrate multimodal data and quantitatively validate cell-type reproducibility. The resulting reference atlas—containing over 56 neuronal cell types that are highly replicable across analysis methods, sequencing technologies and modalities—is a comprehensive molecular and genomic account of the diverse neuronal and non-neuronal cell types in the mouse primary motor cortex. The atlas includes a population of excitatory neurons that resemble pyramidal cells in layer 4 in other cortical regions4. We further discovered thousands of concordant marker genes and gene regulatory elements for these cell types. Our results highlight the complex molecular regulation of cell types in the brain and will directly enable the design of reagents to target specific cell types in the mouse primary motor cortex for functional analysis., The authors describe an integrated atlas of the diverse cell types in the mouse primary motor cortex.

Published
2020

4. Shared and distinct transcriptomic cell types across neocortical areas

Author

Zizhen Yao, Christof Koch, Daniel Hirschstein, Aaron Szafer, Nick Dee, Sheana Parry, Michael Tieu, Michael Hawrylycz, Jeff Goldy, Susan M. Sunkin, Nadiya V. Shapovalova, Amy Bernard, Kanan Lathia, Lucas T. Graybuck, Boaz P. Levi, Trygve E. Bakken, Matthew Kroll, Sarada Viswanathan, Kimberly A. Smith, Thuc Nghi Nguyen, Olivia Fong, Tae Kyung Kim, Tanya L. Daigle, Jeremy A. Miller, Christine Rimorin, Linda Madisen, Karla E. Hirokawa, Tamara Casper, Julie A. Harris, Ali Cetin, Heather A. Sullivan, Bosiljka Tasic, Karel Svoboda, Julie Pendergraft, Osnat Penn, John W. Phillips, Ian R. Wickersham, Ed S. Lein, Loren L. Looger, Peter A. Groblewski, Hongkui Zeng, Allan R. Jones, Rachael Larsen, Emma Garren, Darren Bertagnolli, Michael N. Economo, Eliza Barkan, and Vilas Menon

Subjects
0301 basic medicine, Male, Cell type, Glutamic Acid, Neocortex, Biology, Article, Transcriptome, 03 medical and health sciences, Glutamatergic, Mice, Single-cell analysis, medicine, Animals, GABAergic Neurons, Visual Cortex, Multidisciplinary, Sequence Analysis, RNA, Gene Expression Profiling, Motor Cortex, Gene expression profiling, 030104 developmental biology, medicine.anatomical_structure, Visual cortex, nervous system, Organ Specificity, Female, Single-Cell Analysis, Neuroscience, Biomarkers, Motor cortex
Abstract

The neocortex contains a multitude of cell types that are segregated into layers and functionally distinct areas. To investigate the diversity of cell types across the mouse neocortex, here we analysed 23,822 cells from two areas at distant poles of the mouse neocortex: the primary visual cortex and the anterior lateral motor cortex. We define 133 transcriptomic cell types by deep, single-cell RNA sequencing. Nearly all types of GABA (γ-aminobutyric acid)-containing neurons are shared across both areas, whereas most types of glutamatergic neurons were found in one of the two areas. By combining single-cell RNA sequencing and retrograde labelling, we match transcriptomic types of glutamatergic neurons to their long-range projection specificity. Our study establishes a combined transcriptomic and projectional taxonomy of cortical cell types from functionally distinct areas of the adult mouse cortex.

Published
2017

5. An anatomically comprehensive atlas of the adult human brain transcriptome

Author

Susan M. Sunkin, Preston M. Cartagena, Robert Howard, Christian F. Beckmann, David Feng, Zeb Haradon, Chinh Dang, Angela L. Guillozet-Bongaarts, Derric Williams, Jeff Goldy, Yang Li, Rachel A. Dalley, Tracy Lemon, Darren Bertagnolli, Clifford R. Slaughterbeck, Simon Smith, Steve Horvath, Christof Koch, Amanda Ebbert, Andreas Jeromin, Paul Wohnoutka, Michael Hawrylycz, Andy J. Sodt, Beryl Swanson, H. Ronald Zielke, Zackery L. Riley, John A. Morris, Evan T. Lazarz, Chris Abajian, Allan R. Jones, Mike Chapin, Changkyu Lee, Pedro Adolfo Sequeira, Jay Schulkin, Christopher Lau, Jeremy A. Miller, Tim A. Dolbeare, Ling Li, Nick Dee, Sheana Parry, Barry Daly, Patrick D. Parker, Marty Kinnunen, Amy Bernard, Joshua J. Royall, Vance Faber, John G. Hohmann, Patrick R. Hof, Stephen M. Smith, Suvro Datta, Kimberly A. Smith, Elaine H. Shen, Caroline C. Overly, Ed S. Lein, Jayson M. Jochim, Benjamin W. Gregor, Melissa Reding, M. Mallar Chakravarty, Seth G. N. Grant, Lydia Ng, Jimmy Chong, Marquis P. Vawter, Daniel H. Geschwind, David R. Haynor, Andrew F. Boe, Louie N. van de Lagemaat, David R. Fowler, Magnetic Detection and Imaging, and Faculty of Science and Technology

Subjects
Adult, Male, Cell type, Calbindins, Dopamine, Neocortex, Biology, Hippocampus, Article, Transcriptome, 03 medical and health sciences, Mice, METIS-292322, 0302 clinical medicine, Atlases as Topic, S100 Calcium Binding Protein G, Species Specificity, Databases, Genetic, Transcriptional regulation, medicine, Animals, Humans, RNA, Messenger, Anatomy, Artistic, In Situ Hybridization, 030304 developmental biology, Oligonucleotide Array Sequence Analysis, Genetics, 0303 health sciences, Internet, IR-83002, Multidisciplinary, Anatomical location, Gene Expression Profiling, Brain, Post-Synaptic Density, Human brain, Macaca mulatta, Gene expression profiling, medicine.anatomical_structure, Frontal lobe, Health, Neuroscience, 030217 neurology & neurosurgery
Abstract

Neuroanatomically precise, genome-wide maps of transcript distributions are critical resources to complement genomic sequence data and to correlate functional and genetic brain architecture. Here we describe the generation and analysis of a transcriptional atlas of the adult human brain, comprising extensive histological analysis and comprehensive microarray profiling of ~900 neuroanatomically precise subdivisions in two individuals. Transcriptional regulation varies enormously by anatomical location, with different regions and their constituent cell types displaying robust molecular signatures that are highly conserved between individuals. Analysis of differential gene expression and gene co-expression relationships demonstrates that brain-wide variation strongly reflects the distributions of major cell classes such as neurons, oligodendrocytes, astrocytes and microglia. Local neighbourhood relationships between fine anatomical subdivisions are associated with discrete neuronal subtypes and genes involved with synaptic transmission. The neocortex displays a relatively homogeneous transcriptional pattern, but with distinct features associated selectively with primary sensorimotor cortices and with enriched frontal lobe expression. Notably, the spatial topography of the neocortex is strongly reflected in its molecular topography— the closer two cortical regions, the more similar their transcriptomes. This freely accessible online data resource forms a high-resolution transcriptional baseline for neurogenetic studies of normal and abnormal human brain function.

Published
2012

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