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
N1 - Funding Information:
This research was supported by the Wellcome Trust Investigator Award 103759/Z/14/Z to M.C. This article represents independent research partly funded by the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley National Health Service (NHS) Foundation Trust and King’s College London. We thank Lazar Fleysher, Rafael O’Halloran, Hauke Kolster, Christienne Damatac, Jamie Nagy, Ronald Primm, Pedro Hernandez, and Ignacio Medel for help in acquiring the in vivo macaque datasets, and Leonardo Cerliani for assistance with cynomolgus macaque datasets. We also thank the members of the NatBrainLab and Department of Forensics and Neurodevelopmental Sciences, King’s College London, for feedback and suggestions. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, or the Department of Health. *F.D. and M.C. contributed equally to this work. The authors declare no competing financial interests. Correspondence should be addressed to Marco Catani at m.catani@iop.kcl.ac.uk. https://doi.org/10.1523/JNEUROSCI.1650-18.2019 Copyright © 2020 Barrett et al.
Publisher Copyright:
© Copyright © 2020 Barrett et al.
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
UR - http://www.scopus.com/inward/record.url?scp=85081080277&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.1650-18.2019
DO - 10.1523/JNEUROSCI.1650-18.2019
M3 - Article
C2 - 31949106
AN - SCOPUS:85081080277
VL - 40
SP - 2094
EP - 2107
JO - Journal of Neuroscience
JF - Journal of Neuroscience
SN - 0270-6474
IS - 10
ER -