Molecular and cellular evolution of the primate dorsolateral prefrontal cortex

Shaojie Ma; Mario Skarica; Qian Li; Chuan Xu; Ryan D. Risgaard; Andrew T. N. Tebbenkamp; Xoel Mato-Blanco; Rothem Kovner; Željka Krsnik; Xabier de Martin; Victor Luria; Xavier Martí-Pérez; Dan Liang; Amir Karger; Danielle K. Schmidt; Zachary Gomez-Sanchez; Cai Qi; Kevin T. Gobeske; Sirisha Pochareddy; Ashwin Debnath; Cade J. Hottman; Joshua Spurrier; Leon Teo; Anthony G. Boghdadi; Jihane Homman-Ludiye; John J. Ely; Etienne W. Daadi; Da Mi; Marcel Daadi; Oscar Marín; Patrick R. Hof; Mladen-Roko Rasin; James Bourne; Chet C. Sherwood; Gabriel Santpere; Matthew J. Girgenti; Stephen M. Strittmatter; André M. M. Sousa; Nenad Sestan

doi:10.1126/science.abo7257

Molecular and cellular evolution of the primate dorsolateral prefrontal cortex

Shaojie Ma, Mario Skarica, Qian Li, Chuan Xu, Ryan D. Risgaard, Andrew T. N. Tebbenkamp, Xoel Mato-Blanco, Rothem Kovner, Željka Krsnik, Xabier de Martin, Victor Luria, Xavier Martí-Pérez, Dan Liang, Amir Karger, Danielle K. Schmidt, Zachary Gomez-Sanchez, Cai Qi, Kevin T. Gobeske, Sirisha Pochareddy, Ashwin DebnathCade J. Hottman, Joshua Spurrier, Leon Teo, Anthony G. Boghdadi, Jihane Homman-Ludiye, John J. Ely, Etienne W. Daadi, Da Mi, Marcel Daadi, Oscar Marín, Patrick R. Hof, Mladen-Roko Rasin, James Bourne, Chet C. Sherwood, Gabriel Santpere, Matthew J. Girgenti, Stephen M. Strittmatter, André M. M. Sousa, Nenad Sestan

Developmental Neurobiology

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

25 Citations (Scopus)

Abstract

The granular dorsolateral prefrontal cortex (dlPFC) is an evolutionary specialization of primates that is centrally involved in cognition. We assessed more than 600,000 single-nucleus transcriptomes from adult human, chimpanzee, macaque, and marmoset dlPFC. Although most cell subtypes defined transcriptomically are conserved, we detected several that exist only in a subset of species as well as substantial species-specific molecular differences across homologous neuronal, glial, and non-neural subtypes. The latter are exemplified by human-specific switching between expression of the neuropeptide somatostatin and tyrosine hydroxylase, the rate-limiting enzyme in dopamine production in certain interneurons. The above molecular differences are also illustrated by expression of the neuropsychiatric risk gene FOXP2 , which is human-specific in microglia and primate-specific in layer 4 granular neurons. We generated a comprehensive survey of the dlPFC cellular repertoire and its shared and divergent features in anthropoid primates.

Original language	English
Journal	Science
Volume	377
Issue number	6614
DOIs	https://doi.org/10.1126/science.abo7257
Publication status	Published - 30 Sept 2022

Keywords

Multidisciplinary

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10.1126/science.abo7257

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Ma, S., Skarica, M., Li, Q., Xu, C., Risgaard, R. D., Tebbenkamp, A. T. N., Mato-Blanco, X., Kovner, R., Krsnik, Ž., de Martin, X., Luria, V., Martí-Pérez, X., Liang, D., Karger, A., Schmidt, D. K., Gomez-Sanchez, Z., Qi, C., Gobeske, K. T., Pochareddy, S., ... Sestan, N. (2022). Molecular and cellular evolution of the primate dorsolateral prefrontal cortex. Science, 377(6614). https://doi.org/10.1126/science.abo7257

@article{4d07237a7e6540dd9ba86f80a6aebc07,

title = "Molecular and cellular evolution of the primate dorsolateral prefrontal cortex",

abstract = "The granular dorsolateral prefrontal cortex (dlPFC) is an evolutionary specialization of primates that is centrally involved in cognition. We assessed more than 600,000 single-nucleus transcriptomes from adult human, chimpanzee, macaque, and marmoset dlPFC. Although most cell subtypes defined transcriptomically are conserved, we detected several that exist only in a subset of species as well as substantial species-specific molecular differences across homologous neuronal, glial, and non-neural subtypes. The latter are exemplified by human-specific switching between expression of the neuropeptide somatostatin and tyrosine hydroxylase, the rate-limiting enzyme in dopamine production in certain interneurons. The above molecular differences are also illustrated by expression of the neuropsychiatric risk gene FOXP2 , which is human-specific in microglia and primate-specific in layer 4 granular neurons. We generated a comprehensive survey of the dlPFC cellular repertoire and its shared and divergent features in anthropoid primates.",

keywords = "Multidisciplinary",

author = "Shaojie Ma and Mario Skarica and Qian Li and Chuan Xu and Risgaard, {Ryan D.} and Tebbenkamp, {Andrew T. N.} and Xoel Mato-Blanco and Rothem Kovner and {\v Z}eljka Krsnik and {de Martin}, Xabier and Victor Luria and Xavier Mart{\'i}-P{\'e}rez and Dan Liang and Amir Karger and Schmidt, {Danielle K.} and Zachary Gomez-Sanchez and Cai Qi and Gobeske, {Kevin T.} and Sirisha Pochareddy and Ashwin Debnath and Hottman, {Cade J.} and Joshua Spurrier and Leon Teo and Boghdadi, {Anthony G.} and Jihane Homman-Ludiye and Ely, {John J.} and Daadi, {Etienne W.} and Da Mi and Marcel Daadi and Oscar Mar{\'i}n and Hof, {Patrick R.} and Mladen-Roko Rasin and James Bourne and Sherwood, {Chet C.} and Gabriel Santpere and Girgenti, {Matthew J.} and Strittmatter, {Stephen M.} and Sousa, {Andr{\'e} M. M.} and Nenad Sestan",

year = "2022",

month = sep,

day = "30",

doi = "10.1126/science.abo7257",

language = "English",

volume = "377",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

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Ma, S, Skarica, M, Li, Q, Xu, C, Risgaard, RD, Tebbenkamp, ATN, Mato-Blanco, X, Kovner, R, Krsnik, Ž, de Martin, X, Luria, V, Martí-Pérez, X, Liang, D, Karger, A, Schmidt, DK, Gomez-Sanchez, Z, Qi, C, Gobeske, KT, Pochareddy, S, Debnath, A, Hottman, CJ, Spurrier, J, Teo, L, Boghdadi, AG, Homman-Ludiye, J, Ely, JJ, Daadi, EW, Mi, D, Daadi, M, Marín, O, Hof, PR, Rasin, M-R, Bourne, J, Sherwood, CC, Santpere, G, Girgenti, MJ, Strittmatter, SM, Sousa, AMM & Sestan, N 2022, 'Molecular and cellular evolution of the primate dorsolateral prefrontal cortex', Science, vol. 377, no. 6614. https://doi.org/10.1126/science.abo7257

TY - JOUR

T1 - Molecular and cellular evolution of the primate dorsolateral prefrontal cortex

AU - Ma, Shaojie

AU - Skarica, Mario

AU - Li, Qian

AU - Xu, Chuan

AU - Risgaard, Ryan D.

AU - Tebbenkamp, Andrew T. N.

AU - Mato-Blanco, Xoel

AU - Kovner, Rothem

AU - Krsnik, Željka

AU - de Martin, Xabier

AU - Luria, Victor

AU - Martí-Pérez, Xavier

AU - Liang, Dan

AU - Karger, Amir

AU - Schmidt, Danielle K.

AU - Gomez-Sanchez, Zachary

AU - Qi, Cai

AU - Gobeske, Kevin T.

AU - Pochareddy, Sirisha

AU - Debnath, Ashwin

AU - Hottman, Cade J.

AU - Spurrier, Joshua

AU - Teo, Leon

AU - Boghdadi, Anthony G.

AU - Homman-Ludiye, Jihane

AU - Ely, John J.

AU - Daadi, Etienne W.

AU - Mi, Da

AU - Daadi, Marcel

AU - Marín, Oscar

AU - Hof, Patrick R.

AU - Rasin, Mladen-Roko

AU - Bourne, James

AU - Sherwood, Chet C.

AU - Santpere, Gabriel

AU - Girgenti, Matthew J.

AU - Strittmatter, Stephen M.

AU - Sousa, André M. M.

AU - Sestan, Nenad

PY - 2022/9/30

Y1 - 2022/9/30

N2 - The granular dorsolateral prefrontal cortex (dlPFC) is an evolutionary specialization of primates that is centrally involved in cognition. We assessed more than 600,000 single-nucleus transcriptomes from adult human, chimpanzee, macaque, and marmoset dlPFC. Although most cell subtypes defined transcriptomically are conserved, we detected several that exist only in a subset of species as well as substantial species-specific molecular differences across homologous neuronal, glial, and non-neural subtypes. The latter are exemplified by human-specific switching between expression of the neuropeptide somatostatin and tyrosine hydroxylase, the rate-limiting enzyme in dopamine production in certain interneurons. The above molecular differences are also illustrated by expression of the neuropsychiatric risk gene FOXP2 , which is human-specific in microglia and primate-specific in layer 4 granular neurons. We generated a comprehensive survey of the dlPFC cellular repertoire and its shared and divergent features in anthropoid primates.

AB - The granular dorsolateral prefrontal cortex (dlPFC) is an evolutionary specialization of primates that is centrally involved in cognition. We assessed more than 600,000 single-nucleus transcriptomes from adult human, chimpanzee, macaque, and marmoset dlPFC. Although most cell subtypes defined transcriptomically are conserved, we detected several that exist only in a subset of species as well as substantial species-specific molecular differences across homologous neuronal, glial, and non-neural subtypes. The latter are exemplified by human-specific switching between expression of the neuropeptide somatostatin and tyrosine hydroxylase, the rate-limiting enzyme in dopamine production in certain interneurons. The above molecular differences are also illustrated by expression of the neuropsychiatric risk gene FOXP2 , which is human-specific in microglia and primate-specific in layer 4 granular neurons. We generated a comprehensive survey of the dlPFC cellular repertoire and its shared and divergent features in anthropoid primates.

KW - Multidisciplinary

U2 - 10.1126/science.abo7257

DO - 10.1126/science.abo7257

M3 - Article

SN - 0036-8075

VL - 377

JO - Science

JF - Science

IS - 6614

ER -

Molecular and cellular evolution of the primate dorsolateral prefrontal cortex

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