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

Bibliographic Collection: 
APE, CARTA-Inspired Publication
Publication Type: Journal Article
Authors: Ardesch, Dirk Jan; Scholtens, Lianne H.; Li, Longchuan; Preuss, Todd M.; Rilling, James K.; van den Heuvel, Martijn P.
Year of Publication: 2019
Journal: Proceedings of the National Academy of Sciences
Volume: 116
Issue: 14
Pagination: 7101
Date Published: 2019/04/02
Publication Language: eng

Comparative connectomics provides a powerful framework for studying cross-species differences in brain network architecture, offering important insights into the origin of human brain function. The present study highlights key differences between the human and chimpanzee connectome that have arisen since the divergence from our last common ancestor. Comparative analysis suggests an evolutionary shift in the human connectome toward investment of neural resources in global integration of multimodal information and enhanced functional specialization, potentially supporting the enhancement of complex cognitive function during human evolution. Identification of human connectome adaptations has broad implications for our fundamental understanding of human brain function and may contribute to our knowledge of human-specific mental disorders that involve macroscale changes to the brain’s wiring architecture.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.

DOI: https://doi.org/10.1073/pnas.1818512116
Short Title: Proc Natl Acad Sci USA