Evolutionary Reorganization of the Self-Processing Network across Primates

Abstract

Understanding the evolutionary origins of the structural substrates underlying self-processing is central to elucidating the neural basis of human cognition. Although self-related behaviors differ markedly across primates, the extent to which the underlying neural architecture is conserved or reorganized remains unclear. Here, we investigated shared and species-specific characteristics of the self-processing network (SPN) across humans (n = 46, 19 males), chimpanzees (n = 46, 18 males), and macaques (n = 43, 22 males) using a comparative connectomic framework. We mapped a meta-analysis-derived human SPN onto nonhuman primates within a shared homologous connectivity space defined by conserved white-matter tracts. We compared local microstructural properties and gene expression signatures between humans and macaques and further included chimpanzees as an intermediate evolutionary reference for large-scale structural connectivity. SPN regions exhibited highly similar myelin-sensitive contrast profiles in humans and macaques, accompanied by shared expression patterns of related genes, which were also enriched for human-accelerated brain genes. Large-scale connectivity revealed pronounced species differences, with chimpanzees occupying an intermediate position between humans and macaques. Importantly, evolutionary modifications of the SPN were domain-specific: interoceptive-processing subnetworks showed greater similarity between macaques and chimpanzees; exteroceptive-processing subnetworks showed closer correspondence between chimpanzees and humans; and mental-self-processing subnetworks exhibited greater interspecies differentiation. Moreover, these changes were accompanied by a progressive reorganization of network hubs from insular regions in macaques to cingulate regions in humans. Together, these findings reveal a scale-dependent evolutionary organization of SPN structural substrates and provide a framework for understanding the conservation and reorganization of self-processing architectures across primates.