4.8 Article

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

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.1818512116

Keywords

connectome; evolution; chimpanzee; multimodal; comparative connectomics

Funding

  1. VIDI Grant [452-16-015]
  2. Aard- en levenswetenschappen (ALW) Grant from the Netherlands Organization for Scientific Research [ALWOP.179]
  3. Mental Health and Quality of Life fellowship
  4. National Institutes of Health [P01 AG026423]
  5. National Center for Research Resources Grant [P51RR165, OD P51OD11132]
  6. National Chimpanzee Brain Resource [R24NS092988]
  7. National Institute of Mental Health Grant [P50 MH100029]

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The development of complex cognitive functions during human evolution coincides with pronounced encephalization and expansion of white matter, the brain's infrastructure for region-toregion 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.

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