Longitudinal mapping of the development of cortical thickness and surface area in rhesus macaques during the first three years

Proc Natl Acad Sci U S A. 2023 Aug 8;120(32):e2303313120. doi: 10.1073/pnas.2303313120. Epub 2023 Jul 31.

Abstract

Studying dynamic spatiotemporal patterns of early brain development in macaque monkeys is critical for understanding the cortical organization and evolution in humans, given the phylogenetic closeness between humans and macaques. However, due to huge challenges in the analysis of early brain Magnetic Resonance Imaging (MRI) data typically with extremely low contrast and dynamic imaging appearances, our knowledge of the early macaque cortical development remains scarce. To fill this critical gap, this paper characterizes the early developmental patterns of cortical thickness and surface area in rhesus macaques by leveraging advanced computing tools tailored for early developing brains based on a densely sampled longitudinal dataset with 140 rhesus macaque MRI scans seamlessly covering from birth to 36 mo of age. The average cortical thickness exhibits an inverted U-shaped trajectory with peak thickness at around 4.3 mo of age, which is remarkably in line with the age of peak thickness at 14 mo in humans, considering the around 3:1 age ratio of human to macaque. The total cortical surface area in macaques increases monotonically but with relatively lower expansions than in humans. The spatial distributions of thicker and thinner regions are quite consistent during development, with gyri having a thicker cortex than sulci. By 4 mo of age, over 81% of cortical vertices have reached their peaks in thickness, except for the insula and medial temporal cortices, while most cortical vertices keep expanding in surface area, except for the occipital cortex. These findings provide important insights into early brain development and evolution in primates.

Keywords: cortical development; developmental trajectory; macaque monkeys; spatial patterning.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain
  • Brain Mapping / methods
  • Cerebral Cortex* / pathology
  • Humans
  • Macaca mulatta
  • Magnetic Resonance Imaging* / methods
  • Phylogeny