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

Research output: Contribution to journalArticle

39 Citations (Scopus)

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 languageEnglish (US)
Pages (from-to)1027-1032
Number of pages6
JournalScience
Volume358
Issue number6366
DOIs
StatePublished - Nov 24 2017

Fingerprint

Brain
Genes
Pan troglodytes
Neocortex
Hominidae
Macaca
Brain Diseases
Interneurons
Transcriptome
Primates
Dopamine

All Science Journal Classification (ASJC) codes

  • General

Cite this

Sousa, A. M. M., Zhu, Y., Raghanti, M. A., Kitchen, R. R., Onorati, M., Tebbenkamp, A. T. N., ... 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, André M.M. ; Zhu, Ying ; Raghanti, Mary Ann ; Kitchen, Robert R. ; Onorati, Marco ; Tebbenkamp, Andrew T.N. ; Stutz, Bernardo ; Meyer, Kyle A. ; Li, Mingfeng ; Kawasawa, Yuka Imamura ; Liu, Fuchen ; Perez, Raquel Garcia ; Mele, Marta ; Carvalho, Tiago ; Skarica, Mario ; Gulden, Forrest O. ; Pletikos, Mihovil ; Shibata, Akemi ; Stephenson, Alexa R. ; Edler, Melissa K. ; Ely, John J. ; Elsworth, John D. ; Horvath, Tamas L. ; Hof, Patrick R. ; Hyde, Thomas M. ; Kleinman, Joel E. ; Weinberger, Daniel R. ; Reimers, Mark ; Lifton, Richard P. ; Mane, Shrikant M. ; Noonan, James P. ; State, Matthew W. ; Lein, Ed S. ; Knowles, James A. ; Marques-Bonet, Tomas ; Sherwood, Chet C. ; Gerstein, Mark B. ; Sestan, Nenad. / Molecular and cellular reorganization of neural circuits in the human lineage. In: Science. 2017 ; Vol. 358, No. 6366. pp. 1027-1032.
@article{ab775977e0e2492da7cb18ee3c4d9a18,
title = "Molecular and cellular reorganization of neural circuits in the human lineage",
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",
year = "2017",
month = "11",
day = "24",
doi = "10.1126/science.aan3456",
language = "English (US)",
volume = "358",
pages = "1027--1032",
journal = "Science",
issn = "0036-8075",
publisher = "American Association for the Advancement of Science",
number = "6366",

}

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

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

In: Science, Vol. 358, No. 6366, 24.11.2017, p. 1027-1032.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Molecular and cellular reorganization of neural circuits in the human lineage

AU - Sousa, André M.M.

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

PY - 2017/11/24

Y1 - 2017/11/24

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85034821163&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85034821163&partnerID=8YFLogxK

U2 - 10.1126/science.aan3456

DO - 10.1126/science.aan3456

M3 - Article

C2 - 29170230

AN - SCOPUS:85034821163

VL - 358

SP - 1027

EP - 1032

JO - Science

JF - Science

SN - 0036-8075

IS - 6366

ER -

Sousa AMM, Zhu Y, Raghanti MA, Kitchen RR, Onorati M, Tebbenkamp ATN et al. Molecular and cellular reorganization of neural circuits in the human lineage. Science. 2017 Nov 24;358(6366):1027-1032. https://doi.org/10.1126/science.aan3456