TY - JOUR
T1 - Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees
AU - Ardesch, Dirk Jan
AU - Scholtens, Lianne H.
AU - Li, Longchuan
AU - Preuss, Todd M.
AU - Rilling, James K.
AU - van den Heuvel, Martijn P.
N1 - Copyright © 2019 the Author(s). Published by PNAS.
PY - 2019/4/2
Y1 - 2019/4/2
N2 - 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.
AB - 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.
KW - Chimpanzee
KW - Comparative
KW - Connectome
KW - Connectomics
KW - Evolution
KW - Multimodal
UR - http://www.scopus.com/inward/record.url?scp=85064077057&partnerID=8YFLogxK
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UR - https://www.ncbi.nlm.nih.gov/pubmed/30886094
U2 - https://doi.org/10.1073/pnas.1818512116
DO - https://doi.org/10.1073/pnas.1818512116
M3 - Article
C2 - 30886094
SN - 0027-8424
VL - 116
SP - 7101
EP - 7106
JO - PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
JF - PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
IS - 14
ER -