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

Abstract

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.

Keywords: chimpanzee; comparative connectomics; connectome; evolution; multimodal.

Fig. 1.

Analysis of human-chimpanzee shared connections. The normalized strength of shared connections was obtained in both humans and chimpanzees; the data are shown here as the between-species strength difference averaged per cortical region (A). The cortex was then divided into multimodal association areas, unimodal association areas, and primary areas (B), followed by calculation of weighted edge betweenness centrality of connections linking areas in each of the three categories (C). Weighted edge betweenness centrality captures the proportion of weighted shortest paths between all node pairs (i, j) that pass through a given edge. It incorporates information on both topology and weight (represented here as thickness of the edges) of the connections in the network. In the toy example shown here, edge a has high weight, but its weighted edge betweenness centrality is relatively low owing to its peripheral location in the network. Edge b has lower edge weight than a, but a higher proportion of shortest paths pass through it, resulting in a higher edge betweenness centrality. Finally, edge c has both high weight and a central position in the network with a high proportion of shortest paths passing through it, resulting in high edge betweenness centrality. C, chimpanzee; H, human; NOS, normalized number of streamlines.

Fig. 2.

Human-chimpanzee shared connectivity within and between hemispheres. (A) Circos connectogram (56) depicting human-chimpanzee shared connections, bundled per cortical category (outer circle). The bundle color indicates weighted edge betweenness centrality in humans relative to chimpanzees. The bundle width is proportional to the number of connections contained in each bundle. (B) Weighted edge betweenness centrality of shared connections between multimodal association areas (Left), between unimodal association areas (Middle), and between primary areas (Right) in humans (red) compared with chimpanzees (green). Connections across two cortical categories are shown in SI Appendix, Fig. S1. (C) Weighted edge betweenness centrality of interhemispheric and intrahemispheric shared connections in humans and chimpanzees. (D) Weighted network modularity of shared connectivity in humans and chimpanzees. ***P < 0.001; *P < 0.05; ns, not significant (P > 0.05), C, chimpanzee; H, human; LH, left hemisphere; RH, right hemisphere.

Fig. 3.

Cross-species connectivity differences in tracts related to human language processing. (A) Normalized strength of connections between areas of the language network, averaged per cortical region. Averages are based on connections between language-related areas. (B) Strength of connections between FBA/FCBm and other language-related areas (Left) and strength of connections between FBA/FCBm and the remaining cortical areas (Right). Areas connected to FBA and FCBm not directly involved in language included FA, FB, FC, FDp, IA, IB, PB, PC, and PFD (area descriptions provided in SI Appendix, Table S1). The normalized number of streamlines is shown as connection strength. C, chimpanzee; H, human. ***P < 0.001; **P < 0.01.

Fig. 4.

Network properties of human-specific connections. (A) Schematic representation of left hemisphere connections observed in the human brain but not in the chimpanzee brain (dotted lines indicate interhemispheric connections). A connectogram is shown in SI Appendix, Fig. S3. (B) Division of human-specific connections based on the type of connected cortical areas. (C) Difference in global network efficiency of the human group connectome associated with human-specific connections (n = 33) and fiber length-matched human-chimpanzee shared connections (n = 33). ***P < 0.001; *P < 0.05. (D) Fiber lengths of shared connections (n = 344) and human-specific connections (n = 33).