Human and chimpanzee shared and divergent neurobiological systems for general and specific cognitive brain functions

Abstract

A long-standing topic of interest in human neurosciences is the understanding of the neurobiology underlying human cognition. Less commonly considered is to what extent such systems may be shared with other species. We examined individual variation in brain connectivity in the context of cognitive abilities in chimpanzees (n = 45) and humans in search of a conserved link between cognition and brain connectivity across the two species. Cognitive scores were assessed on a variety of behavioral tasks using chimpanzee- and human-specific cognitive test batteries, measuring aspects of cognition related to relational reasoning, processing speed, and problem solving in both species. We show that chimpanzees scoring higher on such cognitive skills display relatively strong connectivity among brain networks also associated with comparable cognitive abilities in the human group. We also identified divergence in brain networks that serve specialized functions across humans and chimpanzees, such as stronger language connectivity in humans and relatively more prominent connectivity between regions related to spatial working memory in chimpanzees. Our findings suggest that core neural systems of cognition may have evolved before the divergence of chimpanzees and humans, along with potential differential investments in other brain networks relating to specific functional specializations between the two species.

Keywords: MRI; brain; connectome; evolution; intelligence.

Fig. 1.

Study overview. (A) Human Connectome Project (n = 480) data were used to perform a connectome-wide association study (CWAS), correlating the strength of connections in the connectome with a summary score of cognitive performance of the individuals. The regression coefficients of the most strongly associated connections were stored as summary statistics. (B) The stored regression coefficients were multiplied by the corresponding connection strengths of a separate human test set (HCP, n = 572 nonoverlapping subjects) to calculate a polyconnectomic score (PCS), reflecting a predicted cognitive score for every subject in the test set. Predicted scores were correlated with the measured empirical cognitive scores to evaluate the performance of the CWAS analysis in humans. (C) Human CWAS summary statistics were applied to a sample of chimpanzee subjects by multiplying the stored (human) coefficients by the corresponding connection strengths of a chimpanzee dataset. The predicted chimpanzee cognitive scores based on the human CWAS data were correlated with the measured empirical cognitive scores in chimpanzees to evaluate whether strength of connections associated with cognition in humans also predicts individual variation in cognitive performance in chimps. (D) Functional cognitive systems (161 in total, among others, “language” and “working memory”) were mapped by taking functional activation maps from the NeuroSynth database mapped to the DK-114 cortical atlas. Normalized connection strength for the examined functional systems was calculated based on the human and chimpanzee connectome, and compared across species to identify brain functions that displayed a more prominent role in the human versus the chimpanzee brain network. Icons from phylopic.org. Brain plots visualized with Simple brain plot (36).

Fig. 2.

Human-based polyconnectomic scores (PCS) predict cognitive performance in both humans and chimpanzees. (A) Network plot of the top most strongly associated connections visualized on an example human subject. Color corresponds to regression coefficients of the top most strongly associated connections; gray denotes remaining connections. (B) Empirical cognitive scores vs. PCS-predicted cognitive scores in humans (PCS threshold = 29%). (C) Network plot of the top most strongly associated connections visualized on an example chimpanzee subject. (D) Normalized empirical cognitive scores vs. PCS-predicted cognitive scores in chimpanzees (PCS threshold = 29%).

Fig. 3.

Cross-species comparison of network investment in brain functions. (A) Cortical regions included in the language network (Left) and strength of connections between these language regions in humans vs. chimpanzees (Right). (B) Cortical regions included in the working memory network (Left) and strength of connections between these working memory regions in humans vs. chimpanzees (Right). Results of A and B were consistent when using brain maps derived by means of the NeuroSynth database (SI Appendix, Figs. S2 and S3). (C) Relative network strength of all 161 included NeuroSynth terms in humans vs. chimpanzees. Dashed line indicates equal relative strength in humans and chimpanzees. NeuroSynth terms above the dashed line represent brain functions with relatively high network prominence in humans compared with chimpanzees (blue color), while terms below the line represent functions with relatively high network prominence in chimpanzees compared with humans (orange color).