Differences in Frontal Network Anatomy Across Primate Species

• Published in: The Journal of neuroscience Vol. 40; no. 10; pp. 2094 - 2107
• Main Authors: Barrett, Rachel L C, Dawson, Matthew, Dyrby, Tim B, Krug, Kristine, Ptito, Maurice, D'Arceuil, Helen, Croxson, Paula L, Johnson, Philippa J, Howells, Henrietta, Forkel, Stephanie J, Dell'Acqua, Flavio, Catani, Marco
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 04.03.2020
• Subjects: Animals; Anterior commissure; Attention; Brain; Brain Mapping - methods; Chlorocebus aethiops; Cognition; Comparative studies; Cortex (frontal); Diffusion Tensor Imaging - methods; Emotional behavior; Frontal lobe; Frontal Lobe - anatomy & histology; Humans; Image Processing, Computer-Assisted; Macaca fascicularis; Macaca mulatta; Male; Neural Pathways - anatomy & histology; Primates; Social behavior; Somatosensory cortex; Species; Species Specificity; Substantia alba; White Matter - anatomy & histology; comparative anatomy; diffusion MRI; tractography; evolution; connectivity; frontal lobe
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.1650-18.2019

The frontal lobe is central to distinctive aspects of human cognition and behavior. Some comparative studies link this to a larger frontal cortex and even larger frontal white matter in humans compared with other primates, yet others dispute these findings. The discrepancies between studies could be explained by limitations of the methods used to quantify volume differences across species, especially when applied to white matter connections. In this study, we used a novel tractography approach to demonstrate that frontal lobe networks, extending within and beyond the frontal lobes, occupy 66% of total brain white matter in humans and 48% in three monkey species: vervets (Chlorocebus aethiops), rhesus macaque (Macaca mulatta) and cynomolgus macaque (Macaca fascicularis), all male. The simian-human differences in proportional frontal tract volume were significant for projection, commissural, and both intralobar and interlobar association tracts. Among the long association tracts, the greatest difference was found for tracts involved in motor planning, auditory memory, top-down control of sensory information, and visuospatial attention, with no significant differences in frontal limbic tracts important for emotional processing and social behaviour. In addition, we found that a nonfrontal tract, the anterior commissure, had a smaller volume fraction in humans, suggesting that the disproportionally large volume of human frontal lobe connections is accompanied by a reduction in the proportion of some nonfrontal connections. These findings support a hypothesis of an overall rearrangement of brain connections during human evolution. Tractography is a unique tool to map white matter connections in the brains of different species, including humans. This study shows that humans have a greater proportion of frontal lobe connections compared with monkeys, when normalized by total brain white matter volume. In particular, tracts associated with language and higher cognitive functions are disproportionally larger in humans compared with monkeys, whereas other tracts associated with emotional processing are either the same or disproportionally smaller. This supports the hypothesis that the emergence of higher cognitive functions in humans is associated with increased extended frontal connectivity, allowing human brains more efficient cross talk between frontal and other high-order associative areas of the temporal, parietal, and occipital lobes.