Genetic mapping and evolutionary analysis of human-expanded cognitive networks

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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 languageEnglish
Pages (from-to)4839
JournalNature Communications
Volume10
Issue number1
DOIs
Publication statusPublished - 24 Oct 2019

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Brain
Genes
genes
brain
Genetic Loci
Pan troglodytes
Gene Regulatory Networks
Macaca
Autistic Disorder
Dendrites
Intelligence
Synapses
chimpanzees
Schizophrenia
schizophrenia
synapses
expansion
intelligence
dendrites
loci

Cite this

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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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T1 - Genetic mapping and evolutionary analysis of human-expanded cognitive networks

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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DO - 10.1038/s41467-019-12764-8

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