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1. Classification of electrophysiological and morphological neuron types in the mouse visual cortex

Author

David Sandman, Brian Lee, Michael Hawrylycz, Sara Kebede, Tom Egdorf, David Reid, Rob Young, Nivretta Thatra, Stefan Mihalas, David Feng, John W. Phillips, Rebecca de Frates, DiJon Hill, Cliff Slaughterbeck, Samuel R Josephsen, Tamara Casper, Xiaoxiao Liu, Hanchuan Peng, Peter Chong, Colin Farrell, Zhi Zhou, Sheana Parry, Jed Perkins, Brian Long, Susan M. Sunkin, Matthew Kroll, Krissy Brouner, Melissa Gorham, Aaron Szafer, Wayne Wakeman, Hong Gu, Marissa Garwood, Daniel Park, Kristen Hadley, Michael S. Fisher, Lydia Potekhina, Ed Lein, Alice Mukora, Hongkui Zeng, Nick Dee, Aaron Oldre, Lindsay Ng, Thomas Braun, Grace Williams, Tracy Lemon, Julie A. Harris, Medea McGraw, Nadezhda Dotson, Philip R. Nicovich, Amanda Gary, Rusty Mann, Alex M. Henry, Caroline Habel, Samuel Dingman, Katherine E. Link, Nathalie Gaudreault, Gilberto J. Soler-Llavina, Thuc Nghi Nguyen, Nicole Blesie, Bosiljka Tasic, Lydia Ng, Christine Cuhaciyan, Tim Jarsky, Keith B. Godfrey, Costas A. Anastassiou, Kirsten Crichton, Josef Sulc, Martin Schroedter, Dan Castelli, Miranda Robertson, Amy Bernard, Lisa Kim, Songlin Ding, Alyse Doperalski, Nathan W. Gouwens, Herman Tung, Tsega Desta, Corinne Teeter, James Harrington, Jonathan T. Ting, Kris Bickley, Anton Arkhipov, Kiet Ngo, Changkyu Lee, Jim Berg, Agata Budzillo, Emma Garren, Tanya L. Daigle, Christof Koch, Rachel A. Dalley, Eliza Barkan, Staci A. Sorensen, Gabe J. Murphy, Shiella Caldejon, and Naz Taskin

Subjects
0301 basic medicine, Genetically modified mouse, Cell type, Patch-Clamp Techniques, Databases, Factual, Action Potentials, Datasets as Topic, Mice, Transgenic, Biology, Article, Neuron types, Mice, 03 medical and health sciences, chemistry.chemical_compound, 0302 clinical medicine, Genes, Reporter, Biocytin, medicine, Animals, Cell shape, Cell Shape, Visual Cortex, Neurons, General Neuroscience, Laboratory mouse, Electrophysiology, 030104 developmental biology, Visual cortex, medicine.anatomical_structure, chemistry, Transcriptome, Neuroscience, 030217 neurology & neurosurgery
Abstract

Understanding the diversity of cell types in the brain has been an enduring challenge and requires detailed characterization of individual neurons in multiple dimensions. To systematically profile morpho-electric properties of mammalian neurons, we established a single-cell characterization pipeline using standardized patch-clamp recordings in brain slices and biocytin-based neuronal reconstructions. We built a publicly accessible online database, the Allen Cell Types Database, to display these datasets. Intrinsic physiological properties were measured from 1,938 neurons from the adult laboratory mouse visual cortex, morphological properties were measured from 461 reconstructed neurons, and 452 neurons had both measurements available. Quantitative features were used to classify neurons into distinct types using unsupervised methods. We established a taxonomy of morphologically and electrophysiologically defined cell types for this region of the cortex, with 17 electrophysiological types, 38 morphological types and 46 morpho-electric types. There was good correspondence with previously defined transcriptomic cell types and subclasses using the same transgenic mouse lines.

Published
2019
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2. Human cortical expansion involves diversification and specialization of supragranular intratelencephalic-projecting neurons

Author

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

Subjects
0303 health sciences, Cell type, Neocortex, Neurofilament, Biology, Transcriptome, 03 medical and health sciences, Glutamatergic, 0302 clinical medicine, medicine.anatomical_structure, Cortex (anatomy), Specialization (functional), medicine, Neuroscience, 030217 neurology & neurosurgery, Function (biology), 030304 developmental biology
Abstract

The neocortex is disproportionately expanded in human compared to mouse, both in its total volume relative to subcortical structures and in the proportion occupied by supragranular layers that selectively make connections within the cortex and other telencephalic structures. Single-cell transcriptomic analyses of human and mouse cortex show an increased diversity of glutamatergic neuron types in supragranular cortex in human and pronounced gradients as a function of cortical depth. To probe the functional and anatomical correlates of this transcriptomic diversity, we describe a robust Patch-seq platform using neurosurgically-resected human tissues. We characterize the morphological and physiological properties of five transcriptomically defined human glutamatergic supragranular neuron types. Three of these types have properties that are specialized compared to the more homogeneous properties of transcriptomically defined homologous mouse neuron types. The two remaining supragranular neuron types, located exclusively in deep layer 3, do not have clear mouse homologues in supragranular cortex but are transcriptionally most similar to deep layer mouse intratelencephalic-projecting neuron types. Furthermore, we reveal the transcriptomic types in deep layer 3 that express high levels of non-phosphorylated heavy chain neurofilament protein that label long-range neurons known to be selectively depleted in Alzheimer’s disease. Together, these results demonstrate the power of transcriptomic cell type classification, provide a mechanistic underpinning for increased complexity of cortical function in human cortical evolution, and implicate discrete transcriptomic cell types as selectively vulnerable in disease.

Published
2020
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3. Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells

Author

Kris Bickley, Anton Arkhipov, Osnat Penn, Hanchuan Peng, Shea Ransford, Sara Kebede, Kara Ronellenfitch, Matthew Mallory, Krissy Brouner, Madie Hupp, Lydia Ng, Daniel Park, Staci A. Sorensen, Alice Pom, Susan M. Sunkin, Tanya L. Daigle, Fahimeh Baftizadeh, Wayne Wakeman, Aaron Oldre, Amanda Gary, Herman Tung, Brian Lee, Ed S. Lein, Medea McGraw, Rachel A. Dalley, Bosiljka Tasic, Hong Gu, Miranda Robertson, Katherine Baker, Lindsay Ng, David Sandman, Jasmine Bomben, Uygar Sümbül, Tae Kyung Kim, David Reid, Eliza Barkan, Luke Esposito, Kirsten Crichton, DiJon Hill, Zoran Popović, Josef Sulc, Nathan W. Gouwens, Ramkumar Rajanbabu, Lydia Potekhina, Thomas Braun, Alexandra Glandon, Tim Jarsky, Darren Bertagnolli, Tom Egdorf, Olivia Fong, Alice Mukora, Rebecca de Frates, Lauren Ellingwood, Jonathan T. Ting, Gabe J. Murphy, Katelyn Ward, Delissa McMillen, Samuel Dingman Lee, Melissa Gorham, Michelle Maxwell, Clare Gamlin, Zhi Zhou, Jeff Goldy, Rachel Enstrom, Kyla Berry, Colin Farrell, Katherine E. Link, Christine Rimorin, Zizhen Yao, Hongkui Zeng, Kristen Hadley, Augustin Ruiz, Grace Williams, Amy Torkelson, Kimberly A. Smith, Lisa Kim, Aaron Szafer, Nick Dee, Alex M. Henry, Rohan Gala, David Feng, Jessica Trinh, Tamara Casper, Matthew Kroll, Christof Koch, Michael Tieu, Michael Hawrylycz, Lauren Alfiler, Kiet Ngo, Philip R. Nicovich, Thanh Pham, Nadezhda Dotson, Rusty Mann, Tsega Desta, Lucas T. Graybuck, Changkyu Lee, Jim Berg, and Agata Budzillo

Subjects
0303 health sciences, Cell type, biology, Interneuron, General Biochemistry, Genetics and Molecular Biology, Transcriptome, 03 medical and health sciences, Electrophysiology, 0302 clinical medicine, medicine.anatomical_structure, Visual cortex, medicine, biology.protein, GABAergic, Axon, Neuroscience, 030217 neurology & neurosurgery, Parvalbumin, 030304 developmental biology
Abstract

Neurons are frequently classified into distinct types on the basis of structural, physiological, or genetic attributes. To better constrain the definition of neuronal cell types, we characterized the transcriptomes and intrinsic physiological properties of over 4,200 mouse visual cortical GABAergic interneurons and reconstructed the local morphologies of 517 of those neurons. We find that most transcriptomic types (t-types) occupy specific laminar positions within visual cortex, and, for most types, the cells mapping to a t-type exhibit consistent electrophysiological and morphological properties. These properties display both discrete and continuous variation among t-types. Through multimodal integrated analysis, we define 28 met-types that have congruent morphological, electrophysiological, and transcriptomic properties and robust mutual predictability. We identify layer-specific axon innervation pattern as a defining feature distinguishing different met-types. These met-types represent a unified definition of cortical GABAergic interneuron types, providing a systematic framework to capture existing knowledge and bridge future analyses across different modalities.

Published
2020
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4. A comprehensive transcriptional map of primate brain development

Author

Songlin Ding, R.D. Young, Paul Wohnoutka, Anna Hoerder-Suabedissen, Brian L. Youngstrom, Rachel A. Dalley, Terri L. Gilbert, Stephanie Butler, Lydia Potekhina, Jody Parente, Shiella Caldejon, Shu Shi, Kimberly A. Smith, Lon T. Luong, Chinh Dang, Aaron Oldre, Shelby Cate, Emi J. Byrnes, Susan M. Sunkin, Joshua J. Royall, Jefferey Chen, Amanda Ebbert, Jeffrey Rogers, Zeb Haradon, Lindsey Gourley, Ryan May, Naveed Mastan, Aaron Szafer, Chihchau L. Kuan, Kristopher Bickley, Tracy Lemon, Nick Dee, Nerick Mosqueda, Ed S. Lein, David Rosen, Mike Chapin, John W. Phillips, Guangyu Gu, Crissa Bennett, Nadia Dotson, Kate Roll, Ali Kriedberg, Nika Hejazinia, Nadiya V. Shapovalova, Brandon Rogers, Jon Hall, David G. Amaral, Robert Howard, Melaine Sarreal, Sheana Parry, Kaylynn Aiona, Tim A. Dolbeare, Michael Hawrylycz, Allan R. Jones, Robert F. Hevner, Nathan Sjoquist, Tyson Roberts, Marty Kinnunen, Lissette Velasquez, Jay Jochim, Richard A. Gibbs, Anita Carey, Tsega Desta, Jennifer Wu, Kiet Ngo, Julie Nyhus, Julie Pendergraft, Ben W. Gregor, Sheila Shapouri, Amy Bernard, Lydia Ng, Darren Bertagnolli, Eric Olson, Jeff Goldy, Udi Wagley, Changkyu Lee, Christopher Lau, David R. Haynor, Krissy Brouner, Erika Mott, Jeremy A. Miller, Andy J. Sodt, Jeffrey L. Bennett, Jose Melchor, Patrick D. Parker, Cassandra White, Zoltán Molnár, Andrew F. Boe, Zackery L. Riley, Trygve E. Bakken, David Sandman, Garrett Gee, James M. Arnold, Erich Fulfs, Robbie Townsend, Wayne Wakeman, John G. Hohmann, Felix Lee, and Melissa Reding

Subjects
0301 basic medicine, Male, Microcephaly, Aging, Transcription, Genetic, Autism Spectrum Disorder, Neocortex, Molecular neuroscience, Transcriptome, 0302 clinical medicine, Risk Factors, 2.1 Biological and endogenous factors, Primate, Conserved Sequence, Pediatric, Multidisciplinary, biology, Neurogenesis, Brain, Mental Health, medicine.anatomical_structure, Autism spectrum disorder, Neurological, Stem Cell Research - Nonembryonic - Non-Human, Female, Transcription, Biotechnology, General Science & Technology, Intellectual and Developmental Disabilities (IDD), 1.1 Normal biological development and functioning, Article, 03 medical and health sciences, Spatio-Temporal Analysis, Species Specificity, Genetic, biology.animal, Intellectual Disability, Genetics, medicine, Cell Adhesion, Animals, Humans, Cell projection, Human Genome, Neurosciences, Stem Cell Research, medicine.disease, Macaca mulatta, Brain Disorders, 030104 developmental biology, Neurodevelopmental Disorders, Schizophrenia, Neuroscience, 030217 neurology & neurosurgery
Abstract

The transcriptional underpinnings of brain development remain poorly understood, particularly in humans and closely related non-human primates. We describe a high-resolution transcriptional atlas of rhesus monkey (Macaca mulatta) brain development that combines dense temporal sampling of prenatal and postnatal periods with fine anatomical division of cortical and subcortical regions associated with human neuropsychiatric disease. Gene expression changes more rapidly before birth, both in progenitor cells and maturing neurons. Cortical layers and areas acquire adult-like molecular profiles surprisingly late in postnatal development. Disparate cell populations exhibit distinct developmental timing of gene expression, but also unexpected synchrony of processes underlying neural circuit construction including cell projection and adhesion. Candidate risk genes for neurodevelopmental disorders including primary microcephaly, autism spectrum disorder, intellectual disability, and schizophrenia show disease-specific spatiotemporal enrichment within developing neocortex. Human developmental expression trajectories are more similar to monkey than rodent, although approximately 9% of genes show human-specific regulation with evidence for prolonged maturation or neoteny compared to monkey.

Published
2016

5. An anatomic transcriptional atlas of human glioblastoma

Author

Greg Foltz, Parvinder Hothi, Ali Kriedberg, Krissy Brouner, David Feng, Chantal Murthy, Robert Howard, Robert C. Rostomily, David Sandman, Eric Olson, Nadezhda Dotson, Nameeta Shah, Guangyu Gu, Kris Bickley, Lydia Ng, Nika Hejazinia, John W. Phillips, Leonard Kuan, Charles Cobbs, Garrett Gee, Tim A. Dolbeare, Tsega Desta, Shiella Caldejon, Kiet Ngo, Haley Gittleman, Andrew F. Boe, Hwahyung Lee, Rachel A. Dalley, Steven J. White, Chris Lau, Bart Keogh, Graham Stockdale, Lindsey Gourley, Fuhui Long, Darren Bertagnolli, Andrew Sodt, Michael Hawrylycz, Amanda Ebbert, Jill S. Barnholtz-Sloan, David Rosen, Michael S. Fisher, Antonio Iavarone, Ed S. Lein, Stephanie Butler, Patrick J. Cimino, Tracy Lemon, Zack Riley, Allan R. Jones, Megha S Uppin, Mike Chapin, Naveed Mastan, Kimberly A. Smith, Michael E. Berens, Clifford R. Slaughterbeck, Aaron Szafer, Nick Dee, Wayne Wakeman, John G. Hohmann, Benjamin W. Gregor, Suvro Datta, Felix Lee, Ralph B. Puchalski, Melissa Reding, Nadiya V. Shapovalova, Xu Feng, Amy Bernard, Jae Guen Yoon, Erika Mott, Jeremy A. Miller, Justin D. Lathia, Steve R. Nomura, Steven Rostad, Kevin M. Joines, Paul Wohnoutka, Jeff Goldy, Don Marsh, Farrokh Farrokhi, Michael Lankerovich, C. Dirk Keene, and Chinh Dang

Subjects
0301 basic medicine, Poor prognosis, Multidisciplinary, Extramural, Brain Neoplasms, Gene Expression Profiling, Brain tumor, Computational biology, Biology, medicine.disease, Prognosis, Genomic databases, Data resources, Article, nervous system diseases, Gene expression profiling, 03 medical and health sciences, 030104 developmental biology, Atlases as Topic, Databases, Genetic, medicine, Humans, Glioblastoma, neoplasms
Abstract

Anatomically correct tumor genomics Glioblastoma is the most lethal form of human brain cancer. The genomic alterations and gene expression profiles characterizing this tumor type have been widely studied. Puchalski et al. created the Ivy Glioblastoma Atlas, a freely available online resource for the research community. The atlas, a collaborative effort between bioinformaticians and pathologists, maps molecular features of glioblastomas, such as transcriptional signatures, to histologically defined anatomical regions of the tumors. The relationships identified in this atlas, in conjunction with associated databases of clinical and genomic information, could provide new insights into the pathogenesis, diagnosis, and treatment of glioblastoma. Science , this issue p. 660

Published
2016

6. Comprehensive cellular-resolution atlas of the adult human brain

Author

Aaron Szafer, Nick Dee, Paul Wohnoutka, Ani Varjabedian, John W. Phillips, Ed S. Lein, Bergen McMurray, Allison Stevens, Tim A. Dolbeare, Lee S. Tirrell, Susan M. Sunkin, Michael Hawrylycz, Shiella Caldejon, Patrick R. Hof, Christopher Lau, Elaine Shen, Christof Koch, John G. Hohmann, Joshua J. Royall, Lilla Zöllei, James A. Knowles, Phil Lesnar, Melissa Reding, Bruce Fischl, Songlin Ding, Benjamin A.C. Facer, Michelle Write, Lydia Ng, Chinh Dang, Julie Nyhus, Rachel A. Dalley, Allan R. Jones, Nenad Sestan, H. Ronald Zielke, Amy Bernard, Thomas Benner, Zackery L. Riley, David Sandman, Andre van der Kouwe, and Angie Guillozet-Bongaarts

Subjects
0301 basic medicine, cytoarchitecture, DWI, brainstem, 0302 clinical medicine, Neurofilament Proteins, SCR_014329, parvalbumin, Image Processing, Computer-Assisted, Anatomy, Artistic, hypothalamus, 0303 health sciences, medicine.diagnostic_test, General Neuroscience, Brain, amygdala, Human brain, Magnetic Resonance Imaging, brain atlas, Parvalbumins, medicine.anatomical_structure, Cytoarchitecture, Nissl body, symbols, cerebral cortex, Female, Erratum, Research Article, MRI, Adult, cerebellum, Biology, White matter, symbols.namesake, 03 medical and health sciences, hippocampal formation, Neuroimaging, thalamus, medicine, Humans, neurofilament protein, AB_2314904, 030304 developmental biology, Brain atlas, Brain morphometry, Magnetic resonance imaging, Diffusion Magnetic Resonance Imaging, 030104 developmental biology, RRIDs: AB_10000343, Neuroscience, 030217 neurology & neurosurgery
Abstract

Detailed anatomical understanding of the human brain is essential for unraveling its functional architecture, yet current reference atlases have major limitations such as lack of whole‐brain coverage, relatively low image resolution, and sparse structural annotation. We present the first digital human brain atlas to incorporate neuroimaging, high‐resolution histology, and chemoarchitecture across a complete adult female brain, consisting of magnetic resonance imaging (MRI), diffusion‐weighted imaging (DWI), and 1,356 large‐format cellular resolution (1 µm/pixel) Nissl and immunohistochemistry anatomical plates. The atlas is comprehensively annotated for 862 structures, including 117 white matter tracts and several novel cyto‐ and chemoarchitecturally defined structures, and these annotations were transferred onto the matching MRI dataset. Neocortical delineations were done for sulci, gyri, and modified Brodmann areas to link macroscopic anatomical and microscopic cytoarchitectural parcellations. Correlated neuroimaging and histological structural delineation allowed fine feature identification in MRI data and subsequent structural identification in MRI data from other brains. This interactive online digital atlas is integrated with existing Allen Institute for Brain Science gene expression atlases and is publicly accessible as a resource for the neuroscience community. J. Comp. Neurol. 524:3127–3481, 2016. © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

Published
2016
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7. Comprehensive cellular-resolution atlas of the adult human brain

Author

H. Ronald Zielke, Michael Hawrylycz, Patrick R. Hof, Lydia Ng, Phil Lesnar, Thomas Benner, Bruce Fischl, Julie Nyhus, James A. Knowles, Allison Stevens, Christof Koch, David Sandman, Lee S. Tirrell, Songlin Ding, Ed S. Lein, Angie Guillozet-Bongaarts, Zackery L. Riley, Michelle Write, John W. Phillips, Joshua J. Royall, Aaron Szafer, John G. Hohmann, Nick Dee, Bergen McMurray, Benjamin A.C. Facer, Lilla Zöllei, Tim A. Dolbeare, Susan M. Sunkin, Amy Bernard, Melissa Reding, Elaine Shen, Shiella Caldejon, Allan R. Jones, Andre van der Kouwe, Paul Wohnoutka, Ani Varjabedian, Nenad Sestan, Christopher Lau, Chinh Dang, and Rachel A. Dalley

Subjects
0301 basic medicine, 03 medical and health sciences, 030104 developmental biology, 0302 clinical medicine, medicine.anatomical_structure, Cellular resolution, Atlas (anatomy), General Neuroscience, medicine, Human brain, Biology, Neuroscience, 030217 neurology & neurosurgery
Published
2016
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