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

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

83 Scopus citations

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
Article number	eabo7257
Journal	Science
Volume	377
Issue number	6614
DOIs	https://doi.org/10.1126/science.abo7257
State	Published - 30 Sep 2022

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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), Article eabo7257. https://doi.org/10.1126/science.abo7257

@article{b93613f679334e2daab966f0949ec717,

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.",

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 Rasin, {Mladen Roko} 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",

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issn = "0036-8075",

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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, MR, 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, eabo7257. 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.

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U2 - 10.1126/science.abo7257

DO - 10.1126/science.abo7257

M3 - Article

C2 - 36007006

AN - SCOPUS:85139376537

SN - 0036-8075

VL - 377

JO - Science

JF - Science

IS - 6614

M1 - eabo7257

ER -

Molecular and cellular evolution of the primate dorsolateral prefrontal cortex

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