Cargando…

Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees

The development of complex cognitive functions during human evolution coincides with pronounced encephalization and expansion of white matter, the brain’s infrastructure for region-to-region communication. We investigated adaptations of the human macroscale brain network by comparing human brain wir...

Descripción completa

Detalles Bibliográficos
Autores principales: Ardesch, Dirk Jan, Scholtens, Lianne H., Li, Longchuan, Preuss, Todd M., Rilling, James K., van den Heuvel, Martijn P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6452697/
https://www.ncbi.nlm.nih.gov/pubmed/30886094
http://dx.doi.org/10.1073/pnas.1818512116
_version_ 1783409334190866432
author Ardesch, Dirk Jan
Scholtens, Lianne H.
Li, Longchuan
Preuss, Todd M.
Rilling, James K.
van den Heuvel, Martijn P.
author_facet Ardesch, Dirk Jan
Scholtens, Lianne H.
Li, Longchuan
Preuss, Todd M.
Rilling, James K.
van den Heuvel, Martijn P.
author_sort Ardesch, Dirk Jan
collection PubMed
description The development of complex cognitive functions during human evolution coincides with pronounced encephalization and expansion of white matter, the brain’s infrastructure for region-to-region communication. We investigated adaptations of the human macroscale brain network by comparing human brain wiring with that of the chimpanzee, one of our closest living primate relatives. White matter connectivity networks were reconstructed using diffusion-weighted MRI in humans (n = 57) and chimpanzees (n = 20) and then analyzed using network neuroscience tools. We demonstrate higher network centrality of connections linking multimodal association areas in humans compared with chimpanzees, together with a more pronounced modular topology of the human connectome. Furthermore, connections observed in humans but not in chimpanzees particularly link multimodal areas of the temporal, lateral parietal, and inferior frontal cortices, including tracts important for language processing. Network analysis demonstrates a particularly high contribution of these connections to global network integration in the human brain. Taken together, our comparative connectome findings suggest an evolutionary shift in the human brain toward investment of neural resources in multimodal connectivity facilitating neural integration, combined with an increase in language-related connectivity supporting functional specialization.
format Online
Article
Text
id pubmed-6452697
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-64526972019-04-11 Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees Ardesch, Dirk Jan Scholtens, Lianne H. Li, Longchuan Preuss, Todd M. Rilling, James K. van den Heuvel, Martijn P. Proc Natl Acad Sci U S A Biological Sciences The development of complex cognitive functions during human evolution coincides with pronounced encephalization and expansion of white matter, the brain’s infrastructure for region-to-region communication. We investigated adaptations of the human macroscale brain network by comparing human brain wiring with that of the chimpanzee, one of our closest living primate relatives. White matter connectivity networks were reconstructed using diffusion-weighted MRI in humans (n = 57) and chimpanzees (n = 20) and then analyzed using network neuroscience tools. We demonstrate higher network centrality of connections linking multimodal association areas in humans compared with chimpanzees, together with a more pronounced modular topology of the human connectome. Furthermore, connections observed in humans but not in chimpanzees particularly link multimodal areas of the temporal, lateral parietal, and inferior frontal cortices, including tracts important for language processing. Network analysis demonstrates a particularly high contribution of these connections to global network integration in the human brain. Taken together, our comparative connectome findings suggest an evolutionary shift in the human brain toward investment of neural resources in multimodal connectivity facilitating neural integration, combined with an increase in language-related connectivity supporting functional specialization. National Academy of Sciences 2019-04-02 2019-03-18 /pmc/articles/PMC6452697/ /pubmed/30886094 http://dx.doi.org/10.1073/pnas.1818512116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Ardesch, Dirk Jan
Scholtens, Lianne H.
Li, Longchuan
Preuss, Todd M.
Rilling, James K.
van den Heuvel, Martijn P.
Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
title Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
title_full Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
title_fullStr Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
title_full_unstemmed Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
title_short Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
title_sort evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6452697/
https://www.ncbi.nlm.nih.gov/pubmed/30886094
http://dx.doi.org/10.1073/pnas.1818512116
work_keys_str_mv AT ardeschdirkjan evolutionaryexpansionofconnectivitybetweenmultimodalassociationareasinthehumanbraincomparedwithchimpanzees
AT scholtenslianneh evolutionaryexpansionofconnectivitybetweenmultimodalassociationareasinthehumanbraincomparedwithchimpanzees
AT lilongchuan evolutionaryexpansionofconnectivitybetweenmultimodalassociationareasinthehumanbraincomparedwithchimpanzees
AT preusstoddm evolutionaryexpansionofconnectivitybetweenmultimodalassociationareasinthehumanbraincomparedwithchimpanzees
AT rillingjamesk evolutionaryexpansionofconnectivitybetweenmultimodalassociationareasinthehumanbraincomparedwithchimpanzees
AT vandenheuvelmartijnp evolutionaryexpansionofconnectivitybetweenmultimodalassociationareasinthehumanbraincomparedwithchimpanzees