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1. A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain

Author

Yao, Zizhen, van Velthoven, Cindy T. J., Kunst, Michael, Zhang, Meng, McMillen, Delissa, Lee, Changkyu, Jung, Won, Goldy, Jeff, Abdelhak, Aliya, Aitken, Matthew, Baker, Katherine, Baker, Pamela, Barkan, Eliza, Bertagnolli, Darren, Bhandiwad, Ashwin, Bielstein, Cameron, Bishwakarma, Prajal, Campos, Jazmin, Carey, Daniel, Casper, Tamara, Chakka, Anish Bhaswanth, Chakrabarty, Rushil, Chavan, Sakshi, Chen, Min, Clark, Michael, Close, Jennie, Crichton, Kirsten, Daniel, Scott, DiValentin, Peter, Dolbeare, Tim, Ellingwood, Lauren, Fiabane, Elysha, Fliss, Timothy, Gee, James, Gerstenberger, James, Glandon, Alexandra, Gloe, Jessica, Gould, Joshua, Gray, James, Guilford, Nathan, Guzman, Junitta, Hirschstein, Daniel, Ho, Windy, Hooper, Marcus, Huang, Mike, Hupp, Madie, Jin, Kelly, Kroll, Matthew, Lathia, Kanan, Leon, Arielle, Li, Su, Long, Brian, Madigan, Zach, Malloy, Jessica, Malone, Jocelin, Maltzer, Zoe, Martin, Naomi, McCue, Rachel, McGinty, Ryan, Mei, Nicholas, Melchor, Jose, Meyerdierks, Emma, Mollenkopf, Tyler, Moonsman, Skyler, Nguyen, Thuc Nghi, Otto, Sven, Pham, Trangthanh, Rimorin, Christine, Ruiz, Augustin, Sanchez, Raymond, Sawyer, Lane, Shapovalova, Nadiya, Shepard, Noah, Slaughterbeck, Cliff, Sulc, Josef, Tieu, Michael, Torkelson, Amy, Tung, Herman, Valera Cuevas, Nasmil, Vance, Shane, Wadhwani, Katherine, Ward, Katelyn, Levi, Boaz, Farrell, Colin, Young, Rob, Staats, Brian, Wang, Ming-Qiang Michael, Thompson, Carol L., Mufti, Shoaib, Pagan, Chelsea M., Kruse, Lauren, Dee, Nick, Sunkin, Susan M., Esposito, Luke, Hawrylycz, Michael J., Waters, Jack, Ng, Lydia, Smith, Kimberly, Tasic, Bosiljka, Zhuang, Xiaowei, and Zeng, Hongkui

Published
2023
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4. Transcriptomic cytoarchitecture reveals principles of human neocortex organization

Author

Jorstad, Nikolas L., primary, Close, Jennie, additional, Johansen, Nelson, additional, Yanny, Anna Marie, additional, Barkan, Eliza R., additional, Travaglini, Kyle J., additional, Bertagnolli, Darren, additional, Campos, Jazmin, additional, Casper, Tamara, additional, Crichton, Kirsten, additional, Dee, Nick, additional, Ding, Song-Lin, additional, Gelfand, Emily, additional, Goldy, Jeff, additional, Hirschstein, Daniel, additional, Kiick, Katelyn, additional, Kroll, Matthew, additional, Kunst, Michael, additional, Lathia, Kanan, additional, Long, Brian, additional, Martin, Naomi, additional, McMillen, Delissa, additional, Pham, Trangthanh, additional, Rimorin, Christine, additional, Ruiz, Augustin, additional, Shapovalova, Nadiya, additional, Shehata, Soraya, additional, Siletti, Kimberly, additional, Somasundaram, Saroja, additional, Sulc, Josef, additional, Tieu, Michael, additional, Torkelson, Amy, additional, Tung, Herman, additional, Callaway, Edward M., additional, Hof, Patrick R., additional, Keene, C. Dirk, additional, Levi, Boaz P., additional, Linnarsson, Sten, additional, Mitra, Partha P., additional, Smith, Kimberly, additional, Hodge, Rebecca D., additional, Bakken, Trygve E., additional, and Lein, Ed S, additional

Published
2023
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5. Enhancer-AAVs allow genetic access to oligodendrocytes and diverse populations of astrocytes across species

Author

Mich, John K., primary, Sunil, Smrithi, additional, Johansen, Nelson, additional, Martinez, Refugio A., additional, Leytze, Mckaila, additional, Gore, Bryan B., additional, Mahoney, Joseph T., additional, Ben-Simon, Yoav, additional, Bishaw, Yemeserach, additional, Brouner, Krissy, additional, Campos, Jazmin, additional, Canfield, Ryan, additional, Casper, Tamara, additional, Dee, Nick, additional, Egdorf, Tom, additional, Gary, Amanda, additional, Gibson, Shane, additional, Goldy, Jeff, additional, Groce, Erin L., additional, Hirschstein, Daniel, additional, Loftus, Luke, additional, Lusk, Nick, additional, Malone, Jocelin, additional, Martin, Naomi X., additional, Monet, Deja, additional, Omstead, Victoria, additional, Opitz-Araya, Ximena, additional, Oster, Aaron, additional, Pom, Christina A., additional, Potekhina, Lydia, additional, Reding, Melissa, additional, Rimorin, Christine, additional, Ruiz, Augustin, additional, Sedeño-Cortés, Adriana E., additional, Shapovalova, Nadiya V., additional, Taormina, Michael, additional, Taskin, Naz, additional, Tieu, Michael, additional, Valera Cuevas, Nasmil J., additional, Weed, Natalie, additional, Way, Sharon, additional, Yao, Zizhen, additional, McMillen, Delissa A., additional, Kunst, Michael, additional, McGraw, Medea, additional, Thyagarajan, Bargavi, additional, Waters, Jack, additional, Bakken, Trygve E., additional, Yao, Shenqin, additional, Smith, Kimberly A., additional, Svoboda, Karel, additional, Podgorski, Kaspar, additional, Kojima, Yoshiko, additional, Horwitz, Greg D., additional, Zeng, Hongkui, additional, Daigle, Tanya L., additional, Lein, Ed S., additional, Tasic, Bosiljka, additional, Ting, Jonathan T., additional, and Levi, Boaz P., additional

Published
2023
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6. Integrated multimodal cell atlas of Alzheimer’s disease

Author

Gabitto, Mariano I., primary, Travaglini, Kyle J., additional, Rachleff, Victoria M., additional, Kaplan, Eitan S., additional, Long, Brian, additional, Ariza, Jeanelle, additional, Ding, Yi, additional, Mahoney, Joseph T., additional, Dee, Nick, additional, Goldy, Jeff, additional, Melief, Erica J., additional, Brouner, Krissy, additional, Campos, Jazmin, additional, Campos, John, additional, Carr, Ambrose J., additional, Casper, Tamara, additional, Chakrabarty, Rushil, additional, Clark, Michael, additional, Cool, Jonah, additional, Valera Cuevas, Nasmil J., additional, Dalley, Rachel, additional, Darvas, Martin, additional, Ding, Song-Lin, additional, Dolbeare, Tim, additional, Mac Donald, Christine L., additional, Egdorf, Tom, additional, Esposito, Luke, additional, Ferrer, Rebecca, additional, Gala, Rohan, additional, Gary, Amanda, additional, Gloe, Jessica, additional, Guilford, Nathan, additional, Guzman, Junitta, additional, Hirschstein, Daniel, additional, Ho, Windy, additional, Jarksy, Tim, additional, Johansen, Nelson, additional, Kalmbach, Brian E., additional, Keene, Lisa M., additional, Khawand, Sarah, additional, Kilgore, Mitch, additional, Kirkland, Amanda, additional, Kunst, Michael, additional, Lee, Brian R., additional, Malone, Jocelin, additional, Maltzer, Zoe, additional, Martin, Naomi, additional, McCue, Rachel, additional, McMillen, Delissa, additional, Meyerdierks, Emma, additional, Meyers, Kelly P., additional, Mollenkopf, Tyler, additional, Montine, Mark, additional, Nolan, Amber L., additional, Nyhus, Julie, additional, Olsen, Paul A., additional, Pacleb, Maiya, additional, Peña, Nicholas, additional, Pham, Thanh, additional, Pom, Christina Alice, additional, Postupna, Nadia, additional, Ruiz, Augustin, additional, Schantz, Aimee M., additional, Shapovalova, Nadiya V., additional, Sorensen, Staci A., additional, Staats, Brian, additional, Sullivan, Matt, additional, Sunkin, Susan M., additional, Thompson, Carol, additional, Tieu, Michael, additional, Ting, Jonathan, additional, Torkelson, Amy, additional, Tran, Tracy, additional, Wang, Ming-Qiang, additional, Waters, Jack, additional, Wilson, Angela M., additional, Haynor, David, additional, Gatto, Nicole, additional, Jayadev, Suman, additional, Mufti, Shoaib, additional, Ng, Lydia, additional, Mukherjee, Shubhabrata, additional, Crane, Paul K., additional, Latimer, Caitlin S., additional, Levi, Boaz P., additional, Smith, Kimberly, additional, Close, Jennie L., additional, Miller, Jeremy A., additional, Hodge, Rebecca D., additional, Larson, Eric B., additional, Grabowski, Thomas J., additional, Hawrylycz, Michael, additional, Dirk Keene, C., additional, and Lein, Ed S., additional

Published
2023
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7. Integrated multimodal cell atlas of Alzheimer’s disease

Author

Gabitto, Mariano I., Travaglini, Kyle J., Rachleff, Victoria M., Kaplan, Eitan S., Long, Brian, Ariza, Jeanelle, Ding, Yi, Mahoney, Joseph T., Dee, Nick, Goldy, Jeff, Melief, Erica J., Agrawal, Anamika, Kana, Omar, Zhen, Xingjian, Barlow, Samuel T., Brouner, Krissy, Campos, Jazmin, Campos, John, Carr, Ambrose J., Casper, Tamara, Chakrabarty, Rushil, Clark, Michael, Cool, Jonah, Dalley, Rachel, Darvas, Martin, Ding, Song-Lin, Dolbeare, Tim, Egdorf, Tom, Esposito, Luke, Ferrer, Rebecca, Fleckenstein, Lynn E., Gala, Rohan, Gary, Amanda, Gelfand, Emily, Gloe, Jessica, Guilford, Nathan, Guzman, Junitta, Hirschstein, Daniel, Ho, Windy, Hupp, Madison, Jarsky, Tim, Johansen, Nelson, Kalmbach, Brian E., Keene, Lisa M., Khawand, Sarah, Kilgore, Mitchell D., Kirkland, Amanda, Kunst, Michael, Lee, Brian R., Leytze, Mckaila, Mac Donald, Christine L., Malone, Jocelin, Maltzer, Zoe, Martin, Naomi, McCue, Rachel, McMillen, Delissa, Mena, Gonzalo, Meyerdierks, Emma, Meyers, Kelly P., Mollenkopf, Tyler, Montine, Mark, Nolan, Amber L., Nyhus, Julie K., Olsen, Paul A., Pacleb, Maiya, Pagan, Chelsea M., Peña, Nicholas, Pham, Trangthanh, Pom, Christina Alice, Postupna, Nadia, Rimorin, Christine, Ruiz, Augustin, Saldi, Giuseppe A., Schantz, Aimee M., Shapovalova, Nadiya V., Sorensen, Staci A., Staats, Brian, Sullivan, Matt, Sunkin, Susan M., Thompson, Carol, Tieu, Michael, Ting, Jonathan T., Torkelson, Amy, Tran, Tracy, Valera Cuevas, Nasmil J., Walling-Bell, Sarah, Wang, Ming-Qiang, Waters, Jack, Wilson, Angela M., Xiao, Ming, Haynor, David, Gatto, Nicole M., Jayadev, Suman, Mufti, Shoaib, Ng, Lydia, Mukherjee, Shubhabrata, Crane, Paul K., Latimer, Caitlin S., Levi, Boaz P., Smith, Kimberly A., Close, Jennie L., Miller, Jeremy A., Hodge, Rebecca D., Larson, Eric B., Grabowski, Thomas J., Hawrylycz, Michael, Keene, C. Dirk, and Lein, Ed S.

Abstract

Alzheimer’s disease (AD) is the leading cause of dementia in older adults. Although AD progression is characterized by stereotyped accumulation of proteinopathies, the affected cellular populations remain understudied. Here we use multiomics, spatial genomics and reference atlases from the BRAIN Initiative to study middle temporal gyrus cell types in 84 donors with varying AD pathologies. This cohort includes 33 male donors and 51 female donors, with an average age at time of death of 88 years. We used quantitative neuropathology to place donors along a disease pseudoprogression score. Pseudoprogression analysis revealed two disease phases: an early phase with a slow increase in pathology, presence of inflammatory microglia, reactive astrocytes, loss of somatostatin+inhibitory neurons, and a remyelination response by oligodendrocyte precursor cells; and a later phase with exponential increase in pathology, loss of excitatory neurons and Pvalb+and Vip+inhibitory neuron subtypes. These findings were replicated in other major AD studies.

Published
2024
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8. A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain

Author

Yao, Zizhen, primary, van Velthoven, Cindy T. J., additional, Kunst, Michael, additional, Zhang, Meng, additional, McMillen, Delissa, additional, Lee, Changkyu, additional, Jung, Won, additional, Goldy, Jeff, additional, Abdelhak, Aliya, additional, Baker, Pamela, additional, Barkan, Eliza, additional, Bertagnolli, Darren, additional, Campos, Jazmin, additional, Carey, Daniel, additional, Casper, Tamara, additional, Chakka, Anish Bhaswanth, additional, Chakrabarty, Rushil, additional, Chavan, Sakshi, additional, Chen, Min, additional, Clark, Michael, additional, Close, Jennie, additional, Crichton, Kirsten, additional, Daniel, Scott, additional, Dolbeare, Tim, additional, Ellingwood, Lauren, additional, Gee, James, additional, Glandon, Alexandra, additional, Gloe, Jessica, additional, Gould, Joshua, additional, Gray, James, additional, Guilford, Nathan, additional, Guzman, Junitta, additional, Hirschstein, Daniel, additional, Ho, Windy, additional, Jin, Kelly, additional, Kroll, Matthew, additional, Lathia, Kanan, additional, Leon, Arielle, additional, Long, Brian, additional, Maltzer, Zoe, additional, Martin, Naomi, additional, McCue, Rachel, additional, Meyerdierks, Emma, additional, Nguyen, Thuc Nghi, additional, Pham, Trangthanh, additional, Rimorin, Christine, additional, Ruiz, Augustin, additional, Shapovalova, Nadiya, additional, Slaughterbeck, Cliff, additional, Sulc, Josef, additional, Tieu, Michael, additional, Torkelson, Amy, additional, Tung, Herman, additional, Cuevas, Nasmil Valera, additional, Wadhwani, Katherine, additional, Ward, Katelyn, additional, Levi, Boaz, additional, Farrell, Colin, additional, Thompson, Carol L., additional, Mufti, Shoaib, additional, Pagan, Chelsea M., additional, Kruse, Lauren, additional, Dee, Nick, additional, Sunkin, Susan M., additional, Esposito, Luke, additional, Hawrylycz, Michael J., additional, Waters, Jack, additional, Ng, Lydia, additional, Smith, Kimberly A., additional, Tasic, Bosiljka, additional, Zhuang, Xiaowei, additional, and Zeng, Hongkui, additional

Published
2023
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10. Transcriptomic cytoarchitecture reveals principles of human neocortex organization

Author

Jorstad, Nikolas L., primary, Close, Jennie, additional, Johansen, Nelson, additional, Yanny, Anna Marie, additional, Barkan, Eliza R., additional, Travaglini, Kyle J., additional, Bertagnolli, Darren, additional, Campos, Jazmin, additional, Casper, Tamara, additional, Crichton, Kirsten, additional, Dee, Nick, additional, Ding, Song-Lin, additional, Gelfand, Emily, additional, Goldy, Jeff, additional, Hirschstein, Daniel, additional, Kroll, Matthew, additional, Kunst, Michael, additional, Lathia, Kanan, additional, Long, Brian, additional, Martin, Naomi, additional, McMillen, Delissa, additional, Pham, Trangthanh, additional, Rimorin, Christine, additional, Ruiz, Augustin, additional, Shapovalova, Nadiya, additional, Shehata, Soraya, additional, Siletti, Kimberly, additional, Somasundaram, Saroja, additional, Sulc, Josef, additional, Tieu, Michael, additional, Torkelson, Amy, additional, Tung, Herman, additional, Ward, Katelyn, additional, Callaway, Edward M., additional, Hof, Patrick R., additional, Keene, C. Dirk, additional, Levi, Boaz P., additional, Linnarsson, Sten, additional, Mitra, Partha P., additional, Smith, Kimberly, additional, Hodge, Rebecca D., additional, Bakken, Trygve E., additional, and Lein, Ed S., additional

Published
2022
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16. Enhancer-AAVs allow genetic access to oligodendrocytes and diverse populations of astrocytes across species.

Author

Mich JK, Sunil S, Johansen N, Martinez RA, Leytze M, Gore BB, Mahoney JT, Ben-Simon Y, Bishaw Y, Brouner K, Campos J, Canfield R, Casper T, Dee N, Egdorf T, Gary A, Gibson S, Goldy J, Groce EL, Hirschstein D, Loftus L, Lusk N, Malone J, Martin NX, Monet D, Omstead V, Opitz-Araya X, Oster A, Pom CA, Potekhina L, Reding M, Rimorin C, Ruiz A, Sedeño-Cortés AE, Shapovalova NV, Taormina M, Taskin N, Tieu M, Valera Cuevas NJ, Weed N, Way S, Yao Z, McMillen DA, Kunst M, McGraw M, Thyagarajan B, Waters J, Bakken TE, Yao S, Smith KA, Svoboda K, Podgorski K, Kojima Y, Horwitz GD, Zeng H, Daigle TL, Lein ES, Tasic B, Ting JT, and Levi BP

Abstract

Proper brain function requires the assembly and function of diverse populations of neurons and glia. Single cell gene expression studies have mostly focused on characterization of neuronal cell diversity; however, recent studies have revealed substantial diversity of glial cells, particularly astrocytes. To better understand glial cell types and their roles in neurobiology, we built a new suite of adeno-associated viral (AAV)-based genetic tools to enable genetic access to astrocytes and oligodendrocytes. These oligodendrocyte and astrocyte enhancer-AAVs are highly specific (usually > 95% cell type specificity) with variable expression levels, and our astrocyte enhancer-AAVs show multiple distinct expression patterns reflecting the spatial distribution of astrocyte cell types. To provide the best glial-specific functional tools, several enhancer-AAVs were: optimized for higher expression levels, shown to be functional and specific in rat and macaque, shown to maintain specific activity in epilepsy where traditional promoters changed activity, and used to drive functional transgenes in astrocytes including Cre recombinase and acetylcholine-responsive sensor iAChSnFR. The astrocyte-specific iAChSnFR revealed a clear reward-dependent acetylcholine response in astrocytes of the nucleus accumbens during reinforcement learning. Together, this collection of glial enhancer-AAVs will enable characterization of astrocyte and oligodendrocyte populations and their roles across species, disease states, and behavioral epochs.

Published
2023
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17. A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain.

Author

Yao Z, van Velthoven CTJ, Kunst M, Zhang M, McMillen D, Lee C, Jung W, Goldy J, Abdelhak A, Baker P, Barkan E, Bertagnolli D, Campos J, Carey D, Casper T, Chakka AB, Chakrabarty R, Chavan S, Chen M, Clark M, Close J, Crichton K, Daniel S, Dolbeare T, Ellingwood L, Gee J, Glandon A, Gloe J, Gould J, Gray J, Guilford N, Guzman J, Hirschstein D, Ho W, Jin K, Kroll M, Lathia K, Leon A, Long B, Maltzer Z, Martin N, McCue R, Meyerdierks E, Nguyen TN, Pham T, Rimorin C, Ruiz A, Shapovalova N, Slaughterbeck C, Sulc J, Tieu M, Torkelson A, Tung H, Cuevas NV, Wadhwani K, Ward K, Levi B, Farrell C, Thompson CL, Mufti S, Pagan CM, Kruse L, Dee N, Sunkin SM, Esposito L, Hawrylycz MJ, Waters J, Ng L, Smith KA, Tasic B, Zhuang X, and Zeng H

Abstract

The mammalian brain is composed of millions to billions of cells that are organized into numerous cell types with specific spatial distribution patterns and structural and functional properties. An essential step towards understanding brain function is to obtain a parts list, i.e., a catalog of cell types, of the brain. Here, we report a comprehensive and high-resolution transcriptomic and spatial cell type atlas for the whole adult mouse brain. The cell type atlas was created based on the combination of two single-cell-level, whole-brain-scale datasets: a single-cell RNA-sequencing (scRNA-seq) dataset of ~7 million cells profiled, and a spatially resolved transcriptomic dataset of ~4.3 million cells using MERFISH. The atlas is hierarchically organized into five nested levels of classification: 7 divisions, 32 classes, 306 subclasses, 1,045 supertypes and 5,200 clusters. We systematically analyzed the neuronal, non-neuronal, and immature neuronal cell types across the brain and identified a high degree of correspondence between transcriptomic identity and spatial specificity for each cell type. The results reveal unique features of cell type organization in different brain regions, in particular, a dichotomy between the dorsal and ventral parts of the brain: the dorsal part contains relatively fewer yet highly divergent neuronal types, whereas the ventral part contains more numerous neuronal types that are more closely related to each other. We also systematically characterized cell-type specific expression of neurotransmitters, neuropeptides, and transcription factors. The study uncovered extraordinary diversity and heterogeneity in neurotransmitter and neuropeptide expression and co-expression patterns in different cell types across the brain, suggesting they mediate a myriad of modes of intercellular communications. Finally, we found that transcription factors are major determinants of cell type classification in the adult mouse brain and identified a combinatorial transcription factor code that defines cell types across all parts of the brain. The whole-mouse-brain transcriptomic and spatial cell type atlas establishes a benchmark reference atlas and a foundational resource for deep and integrative investigations of cell type and circuit function, development, and evolution of the mammalian brain., Competing Interests: Competing Interests X.Z. is a co-founder and consultant of Vizgen.

Published
2023
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