Comparative Primate Connectomics

Abstract

A connectome is a comprehensive map of neural connections of a species nervous system. While recent work has begun comparing connectomes across a wide breadth of species, we present here a more detailed and specific comparison of connectomes across the primate order. Long-range connections are thought to improve communication efficiency and thus brain function but are costly in terms of energy and space utilization. Methods for measuring connectivity in the brain include measuring white matter volume, histological cell counting, anatomical tract tracing, diffusion-weighted imaging and tractography, and functional connectivity in MRI. Comparisons of global white matter connectivity suggest that larger primate brains are less well connected than smaller primate brains, but that humans have more connections than expected for our cortical neuron number, which may be concentrated in the prefrontal cortex. Although there is significant overlap in structural connectivity between humans and nonhuman primates, human-specific connections are found in cortical areas involved with language, imitation, and tool use. Similar to structural connectivity, there is also widespread overlap between humans and macaques in resting state functional connectivity. However, there are again a number of human-specific connections in cortical regions involved in language, tool use, and empathy. Comparative connectomics also offers the opportunity to detect specializations of connectivity in other primate species besides humans. Future research should capitalize on the ability of diffusion tractography to measure connectivity in postmortem brains that could expand the representation of species beyond humans, chimpanzees, and rhesus macaques, and facilitate identification of connectivity-based adaptations to different social and ecological niches. This work will require careful attention to establishing cortical homologies across species and to improving tractography methods to limit detection of false-positive and false-negative connections. Finally, it will be important to attempt to establish the functional significance of variation in connectivity profiles by examining how these covary with behavior and cognition both across and within species.