TY - JOUR
T1 - Differences in frontal network anatomy across primate species
AU - Barrett, Rachel L.C.
AU - Dawson, Matthew
AU - Dyrby, Tim B.
AU - Krug, Kristine
AU - Ptito, Maurice
AU - D'Arceuil, Helen
AU - Croxson, Paula L.
AU - Johnson, Philippa J.
AU - Howells, Henrietta
AU - Forkel, Stephanie J.
AU - Dell'Acqua, Flavio
AU - Catani, Marco
PY - 2020/3/4
Y1 - 2020/3/4
N2 - 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.
AB - 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.
KW - Comparative anatomy
KW - Connectivity
KW - Diffusion MRI
KW - Evolution
KW - Frontal lobe
KW - Tractography
U2 - 10.1523/JNEUROSCI.1650-18.2019
DO - 10.1523/JNEUROSCI.1650-18.2019
M3 - Journal article
C2 - 31949106
AN - SCOPUS:85081080277
SN - 0270-6474
VL - 40
SP - 2094
EP - 2107
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 10
ER -