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
J. Neurosci.. 2020-01-16; 40(10): 2094-2107
DOI: 10.1523/jneurosci.1650-18.2019

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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.SIGNIFICANCE STATEMENT 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.


Auteurs Bordeaux Neurocampus