The Evolution of Language‐Related Long Association Pathways: A Comparative Study Between Humans and Rhesus Macaques

Abstract

The human brain stands out from other primates for its large size. After the split with our last common ancestor (LCA) with chimpanzees—our closest living relative—, the hominin brain expanded threefold, and the frontal and parietal operculum underwent substantial morphological reorganization, likely reflecting language acquisition in our species. The increase of brain size was not homogeneous: the inferior frontal and the parietal areas had a disproportionally large expansion while the occipital lobe retained its absolute size. These evolutionary changes are even more pronounced when human brains are compared to those of Old World monkeys. However, the amount of change in long association pathways within these highly modified regions is not well understood.This study aims to identify differences and similarities in homologous pathways of the human language network in the macaque brain. We hypothesize that language‐related pathways projecting to/from the inferior frontal and parietal areas will exhibit substantial reorganization in humans.Using state‐of‐the‐art, publicly available diffusion MRI data of a healthy (in vivo) adult human (MGH‐USC) [1] and 6 ex vivo rhesus macaque (Oxford University, PRIME‐DE) [2] brains, we reconstructed and virtually dissected in DSI Studio three association pathways: the arcuate fasciculus (AF), the frontal aslant tract (FAT), and the parietal‐projecting portion of the extreme capsule (pEmC). We show that the course and terminal projections of the FAT (inferior frontal and supplementary motor area) and the pEmC (superior parietal lobule and frontal cortical areas) are highly evolutionarily preserved in both species despite their crucial role in language in humans. In stark contrast, the AF underwent a major modification in its posterior segment, as previously reported.Our results suggest that evolutionary changes in the regional volumetric morphology of the brain do not necessarily imply similarly large changes in the relative volumes and trajectories of underlying white matter pathways. In addition, the current results suggest that the structural basis of human language functions already existed, at least to some extent, in the LCA with macaques. Functional and behavioral studies are needed to understand the role of this white matter network in both species.