Genetic mapping and evolutionary analysis of human-expanded cognitive networks

Yongbin Wei; Siemon C de Lange; Lianne H Scholtens; Kyoko Watanabe; Dirk Jan Ardesch; Philip R Jansen; Jeanne E Savage; Longchuan Li; Todd M Preuss; James K Rilling; Danielle Posthuma; Martijn P van den Heuvel

doi:10.1038/s41467-019-12764-8

Genetic mapping and evolutionary analysis of human-expanded cognitive networks

Yongbin Wei, Siemon C de Lange, Lianne H Scholtens, Kyoko Watanabe, Dirk Jan Ardesch, Philip R Jansen, Jeanne E Savage, Longchuan Li, Todd M Preuss, James K Rilling, Danielle Posthuma, Martijn P van den Heuvel

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Cognitive brain networks such as the default-mode network (DMN), frontoparietal network, and salience network, are key functional networks of the human brain. Here we show that the rapid evolutionary cortical expansion of cognitive networks in the human brain, and most pronounced the DMN, runs parallel with high expression of human-accelerated genes (HAR genes). Using comparative transcriptomics analysis, we present that HAR genes are differentially more expressed in higher-order cognitive networks in humans compared to chimpanzees and macaques and that genes with high expression in the DMN are involved in synapse and dendrite formation. Moreover, HAR and DMN genes show significant associations with individual variations in DMN functional activity, intelligence, sociability, and mental conditions such as schizophrenia and autism. Our results suggest that the expansion of higher-order functional networks subserving increasing cognitive properties has been an important locus of genetic changes in recent human brain evolution.

Original language	English
Article number	4839
Pages (from-to)	4839
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12764-8
Publication status	Published - 24 Oct 2019

Funding

Funders	Funder number
Common Fund of the
Dutch Brain Foundation
Dutch National computing and Networking Services SURFsara
NIH Institutes
NWO VICI 453-14-005	VICI 453-14-005
National Chimpanzee Brain Resource	R24NS092988
Netherlands Organization for Scientific Research
Netherlands Scientific Organization	480-05-003
Office of Research Infrastructure Programs/OD	Programs/OD P51OD11132
Office of the
SSWO	s14-27
Sophia Foundation for Scientific Research
The Netherlands Organization for Scientific Research
VIDI	452-16-015
WU-Minn Consortium	1U54MH091657
National Institute of Mental Health	MH100029
National Heart, Lung, and Blood Institute	NIDA
National Human Genome Research Institute
National Cancer Institute
National Institute of Neurological Disorders and Stroke
NIH Blueprint for Neuroscience Research
McDonnell Center for Systems Neuroscience
Yerkes National Primate Research Center, Emory University
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	VIDI (452-16-015), ALW open (ALWOP.179)
China Scholarship Council	201506040039
National Health Research Institutes	P01AG026423, P51RR165

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@article{d8dae835e7c741e4851110cb8948f28d,

title = "Genetic mapping and evolutionary analysis of human-expanded cognitive networks",

abstract = "Cognitive brain networks such as the default-mode network (DMN), frontoparietal network, and salience network, are key functional networks of the human brain. Here we show that the rapid evolutionary cortical expansion of cognitive networks in the human brain, and most pronounced the DMN, runs parallel with high expression of human-accelerated genes (HAR genes). Using comparative transcriptomics analysis, we present that HAR genes are differentially more expressed in higher-order cognitive networks in humans compared to chimpanzees and macaques and that genes with high expression in the DMN are involved in synapse and dendrite formation. Moreover, HAR and DMN genes show significant associations with individual variations in DMN functional activity, intelligence, sociability, and mental conditions such as schizophrenia and autism. Our results suggest that the expansion of higher-order functional networks subserving increasing cognitive properties has been an important locus of genetic changes in recent human brain evolution.",

author = "Yongbin Wei and {de Lange}, {Siemon C} and Scholtens, {Lianne H} and Kyoko Watanabe and Ardesch, {Dirk Jan} and Jansen, {Philip R} and Savage, {Jeanne E} and Longchuan Li and Preuss, {Todd M} and Rilling, {James K} and Danielle Posthuma and {van den Heuvel}, {Martijn P}",

year = "2019",

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doi = "10.1038/s41467-019-12764-8",

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AU - Wei, Yongbin

AU - de Lange, Siemon C

AU - Scholtens, Lianne H

AU - Watanabe, Kyoko

AU - Ardesch, Dirk Jan

AU - Jansen, Philip R

AU - Savage, Jeanne E

AU - Li, Longchuan

AU - Preuss, Todd M

AU - Rilling, James K

AU - Posthuma, Danielle

AU - van den Heuvel, Martijn P

PY - 2019/10/24

Y1 - 2019/10/24

N2 - Cognitive brain networks such as the default-mode network (DMN), frontoparietal network, and salience network, are key functional networks of the human brain. Here we show that the rapid evolutionary cortical expansion of cognitive networks in the human brain, and most pronounced the DMN, runs parallel with high expression of human-accelerated genes (HAR genes). Using comparative transcriptomics analysis, we present that HAR genes are differentially more expressed in higher-order cognitive networks in humans compared to chimpanzees and macaques and that genes with high expression in the DMN are involved in synapse and dendrite formation. Moreover, HAR and DMN genes show significant associations with individual variations in DMN functional activity, intelligence, sociability, and mental conditions such as schizophrenia and autism. Our results suggest that the expansion of higher-order functional networks subserving increasing cognitive properties has been an important locus of genetic changes in recent human brain evolution.

AB - Cognitive brain networks such as the default-mode network (DMN), frontoparietal network, and salience network, are key functional networks of the human brain. Here we show that the rapid evolutionary cortical expansion of cognitive networks in the human brain, and most pronounced the DMN, runs parallel with high expression of human-accelerated genes (HAR genes). Using comparative transcriptomics analysis, we present that HAR genes are differentially more expressed in higher-order cognitive networks in humans compared to chimpanzees and macaques and that genes with high expression in the DMN are involved in synapse and dendrite formation. Moreover, HAR and DMN genes show significant associations with individual variations in DMN functional activity, intelligence, sociability, and mental conditions such as schizophrenia and autism. Our results suggest that the expansion of higher-order functional networks subserving increasing cognitive properties has been an important locus of genetic changes in recent human brain evolution.

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