Molecular and cellular reorganization of neural circuits in the human lineage

André M.M. Sousa; Ying Zhu; Mary Ann Raghanti; Robert R. Kitchen; Marco Onorati; Andrew T.N. Tebbenkamp; Bernardo Stutz; Kyle A. Meyer; Mingfeng Li; Yuka Imamura Kawasawa; Fuchen Liu; Raquel Garcia Perez; Marta Mele; Tiago Carvalho; Mario Skarica; Forrest O. Gulden; Mihovil Pletikos; Akemi Shibata; Alexa R. Stephenson; Melissa K. Edler; John J. Ely; John D. Elsworth; Tamas L. Horvath; Patrick R. Hof; Thomas M. Hyde; Joel E. Kleinman; Daniel R. Weinberger; Mark Reimers; Richard P. Lifton; Shrikant M. Mane; James P. Noonan; Matthew W. State; Ed S. Lein; James A. Knowles; Tomas Marques-Bonet; Chet C. Sherwood; Mark B. Gerstein; Nenad Sestan

doi:10.1126/science.aan3456

Molecular and cellular reorganization of neural circuits in the human lineage

André M.M. Sousa, Ying Zhu, Mary Ann Raghanti, Robert R. Kitchen, Marco Onorati, Andrew T.N. Tebbenkamp, Bernardo Stutz, Kyle A. Meyer, Mingfeng Li, Yuka Imamura Kawasawa, Fuchen Liu, Raquel Garcia Perez, Marta Mele, Tiago Carvalho, Mario Skarica, Forrest O. Gulden, Mihovil Pletikos, Akemi Shibata, Alexa R. Stephenson, Melissa K. EdlerJohn J. Ely, John D. Elsworth, Tamas L. Horvath, Patrick R. Hof, Thomas M. Hyde, Joel E. Kleinman, Daniel R. Weinberger, Mark Reimers, Richard P. Lifton, Shrikant M. Mane, James P. Noonan, Matthew W. State, Ed S. Lein, James A. Knowles, Tomas Marques-Bonet, Chet C. Sherwood, Mark B. Gerstein, Nenad Sestan

School of Medicine

Research output: Contribution to journal › Article › peer-review

77 Scopus citations

Abstract

To better understand the molecular and cellular differences in brain organization between human and nonhuman primates, we performed transcriptome sequencing of 16 regions of adult human, chimpanzee, and macaque brains. Integration with human single-cell transcriptomic data revealed global, regional, and cell-type–specific species expression differences in genes representing distinct functional categories. We validated and further characterized the human specificity of genes enriched in distinct cell types through histological and functional analyses, including rare subpallial-derived interneurons expressing dopamine biosynthesis genes enriched in the human striatum and absent in the nonhuman African ape neocortex. Our integrated analysis of the generated data revealed diverse molecular and cellular features of the phylogenetic reorganization of the human brain across multiple levels, with relevance for brain function and disease.

Original language	English (US)
Pages (from-to)	1027-1032
Number of pages	6
Journal	Science
Volume	358
Issue number	6366
DOIs	https://doi.org/10.1126/science.aan3456
State	Published - Nov 24 2017

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Sousa, A. M. M., Zhu, Y., Raghanti, M. A., Kitchen, R. R., Onorati, M., Tebbenkamp, A. T. N., Stutz, B., Meyer, K. A., Li, M., Kawasawa, Y. I., Liu, F., Perez, R. G., Mele, M., Carvalho, T., Skarica, M., Gulden, F. O., Pletikos, M., Shibata, A., Stephenson, A. R., ... Sestan, N. (2017). Molecular and cellular reorganization of neural circuits in the human lineage. Science, 358(6366), 1027-1032. https://doi.org/10.1126/science.aan3456

Sousa, AMM, Zhu, Y, Raghanti, MA, Kitchen, RR, Onorati, M, Tebbenkamp, ATN, Stutz, B, Meyer, KA, Li, M, Kawasawa, YI, Liu, F, Perez, RG, Mele, M, Carvalho, T, Skarica, M, Gulden, FO, Pletikos, M, Shibata, A, Stephenson, AR, Edler, MK, Ely, JJ, Elsworth, JD, Horvath, TL, Hof, PR, Hyde, TM, Kleinman, JE , Weinberger, DR, Reimers, M, Lifton, RP, Mane, SM, Noonan, JP, State, MW, Lein, ES, Knowles, JA, Marques-Bonet, T, Sherwood, CC, Gerstein, MB & Sestan, N 2017, 'Molecular and cellular reorganization of neural circuits in the human lineage', Science, vol. 358, no. 6366, pp. 1027-1032. https://doi.org/10.1126/science.aan3456

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abstract = "To better understand the molecular and cellular differences in brain organization between human and nonhuman primates, we performed transcriptome sequencing of 16 regions of adult human, chimpanzee, and macaque brains. Integration with human single-cell transcriptomic data revealed global, regional, and cell-type–specific species expression differences in genes representing distinct functional categories. We validated and further characterized the human specificity of genes enriched in distinct cell types through histological and functional analyses, including rare subpallial-derived interneurons expressing dopamine biosynthesis genes enriched in the human striatum and absent in the nonhuman African ape neocortex. Our integrated analysis of the generated data revealed diverse molecular and cellular features of the phylogenetic reorganization of the human brain across multiple levels, with relevance for brain function and disease.",

author = "Sousa, {Andr{\'e} M.M.} and Ying Zhu and Raghanti, {Mary Ann} and Kitchen, {Robert R.} and Marco Onorati and Tebbenkamp, {Andrew T.N.} and Bernardo Stutz and Meyer, {Kyle A.} and Mingfeng Li and Kawasawa, {Yuka Imamura} and Fuchen Liu and Perez, {Raquel Garcia} and Marta Mele and Tiago Carvalho and Mario Skarica and Gulden, {Forrest O.} and Mihovil Pletikos and Akemi Shibata and Stephenson, {Alexa R.} and Edler, {Melissa K.} and Ely, {John J.} and Elsworth, {John D.} and Horvath, {Tamas L.} and Hof, {Patrick R.} and Hyde, {Thomas M.} and Kleinman, {Joel E.} and Weinberger, {Daniel R.} and Mark Reimers and Lifton, {Richard P.} and Mane, {Shrikant M.} and Noonan, {James P.} and State, {Matthew W.} and Lein, {Ed S.} and Knowles, {James A.} and Tomas Marques-Bonet and Sherwood, {Chet C.} and Gerstein, {Mark B.} and Nenad Sestan",

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AU - Zhu, Ying

AU - Raghanti, Mary Ann

AU - Kitchen, Robert R.

AU - Onorati, Marco

AU - Tebbenkamp, Andrew T.N.

AU - Stutz, Bernardo

AU - Meyer, Kyle A.

AU - Li, Mingfeng

AU - Kawasawa, Yuka Imamura

AU - Liu, Fuchen

AU - Perez, Raquel Garcia

AU - Mele, Marta

AU - Carvalho, Tiago

AU - Skarica, Mario

AU - Gulden, Forrest O.

AU - Pletikos, Mihovil

AU - Shibata, Akemi

AU - Stephenson, Alexa R.

AU - Edler, Melissa K.

AU - Ely, John J.

AU - Elsworth, John D.

AU - Horvath, Tamas L.

AU - Hof, Patrick R.

AU - Hyde, Thomas M.

AU - Kleinman, Joel E.

AU - Weinberger, Daniel R.

AU - Reimers, Mark

AU - Lifton, Richard P.

AU - Mane, Shrikant M.

AU - Noonan, James P.

AU - State, Matthew W.

AU - Lein, Ed S.

AU - Knowles, James A.

AU - Marques-Bonet, Tomas

AU - Sherwood, Chet C.

AU - Gerstein, Mark B.

AU - Sestan, Nenad

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Molecular and cellular reorganization of neural circuits in the human lineage

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