Differences in frontal network anatomy across primate species

Rachel L.C. Barrett, Matthew Dawson, Tim B. Dyrby, Kristine Krug, Maurice Ptito, Helen D'Arceuil, Paula L. Croxson, Philippa J. Johnson, Henrietta Howells, Stephanie J. Forkel, Flavio Dell'Acqua, Marco Catani*

*Corresponding author for this work

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Abstract

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.

Original languageEnglish
JournalJournal of neuroscience
Volume40
Issue number10
Pages (from-to)2094-2107
Number of pages14
ISSN0270-6474
DOIs
Publication statusPublished - 4 Mar 2020

Keywords

  • Comparative anatomy
  • Connectivity
  • Diffusion MRI
  • Evolution
  • Frontal lobe
  • Tractography

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