Convergent and divergent connectivity patterns of the arcuate fasciculus in macaques and humans

TL;DR

This study compares the connectivity patterns of the arcuate fasciculus in macaques and humans, revealing evolutionary differences that may underpin advanced language abilities in humans.

Contribution

It combines cross-scale neuroanatomical tracing and high-resolution MRI to elucidate species-specific differences in arcuate fasciculus connectivity.

Findings

Macaque AF originates in temporal-parietal cortex and projects to prefrontal regions.

Human AF shows expanded connectivity into middle temporal gyrus and stronger frontoparietal links.

Differences likely support the evolution of complex language networks in humans.

Abstract

The organization and connectivity of the arcuate fasciculus (AF) in nonhuman primates remain contentious, especially concerning how its anatomy diverges from that of humans. Here, we combined cross-scale single-neuron tracing - using viral-based genetic labeling and fluorescence micro-optical sectioning tomography in macaques (n = 4; age 3 - 11 years) - with whole-brain tractography from 11.7T diffusion MRI. Complemented by spectral embedding analysis of 7.0T MRI in humans, we performed a comparative connectomic analysis of the AF across species. We demonstrate that the macaque AF originates in the temporal-parietal cortex, traverses the auditory cortex and parietal operculum, and projects into prefrontal regions. In contrast, the human AF exhibits greater expansion into the middle temporal gyrus and stronger prefrontal and parietal operculum connectivity - divergences quantified by Kullback-Leibler analysis that likely underpin the evolutionary specialization of human language networks. These interspecies differences - particularly the human AF's broader temporal integration and strengthened frontoparietal linkages - suggest a connectivity-based substrate for the emergence of advanced language processing unique to humans. Furthermore, our findings offer a neuroanatomical framework for understanding AF-related disorders such as aphasia and dyslexia, where aberrant connectivity disrupts language function.