Maternal Interleukin-6 Is Associated With Macaque Offspring Amygdala Development and Behavior

Julian S.B. Ramirez, Alice M. Graham, Jacqueline R. Thompson, Jennifer Y. Zhu, Darrick Sturgeon, Jennifer L. Bagley, Elina Thomas, Samantha Papadakis, Muhammed Bah, Anders Perrone, Eric Earl, Oscar Miranda-Dominguez, Eric Feczko, Eric J. Fombonne, David G. Amaral, Joel T. Nigg, Elinor L. Sullivan, Damien A. Fair

Research output: Contribution to journalArticle

Abstract

Human and animal cross-sectional studies have shown that maternal levels of the inflammatory cytokine interleukin-6 (IL-6) may compromise brain phenotypes assessed at single time points. However, how maternal IL-6 associates with the trajectory of brain development remains unclear. We investigated whether maternal IL-6 levels during pregnancy relate to offspring amygdala volume development and anxiety-like behavior in Japanese macaques. Magnetic resonance imaging (MRI) was administered to 39 Japanese macaque offspring (Female: 18), providing at least one or more time points at 4, 11, 21, and 36 months of age with a behavioral assessment at 11 months of age. Increased maternal third trimester plasma IL-6 levels were associated with offspring's smaller left amygdala volume at 4 months, but with more rapid amygdala growth from 4 to 36 months. Maternal IL-6 predicted offspring anxiety-like behavior at 11 months, which was mediated by reduced amygdala volumes in the model's intercept (i.e., 4 months). The results increase our understanding of the role of maternal inflammation in the development of neurobehavioral disorders by detailing the associations of a commonly examined inflammatory indicator, IL-6, on amygdala volume growth over time, and anxiety-like behavior.

Original languageEnglish (US)
Pages (from-to)1573-1585
Number of pages13
JournalCerebral cortex (New York, N.Y. : 1991)
Volume30
Issue number3
DOIs
StatePublished - Mar 14 2020

Keywords

  • anxiety
  • inflammation
  • maternal environment
  • MRI
  • neurodevelopment

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience

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  • Cite this

    Ramirez, J. S. B., Graham, A. M., Thompson, J. R., Zhu, J. Y., Sturgeon, D., Bagley, J. L., Thomas, E., Papadakis, S., Bah, M., Perrone, A., Earl, E., Miranda-Dominguez, O., Feczko, E., Fombonne, E. J., Amaral, D. G., Nigg, J. T., Sullivan, E. L., & Fair, D. A. (2020). Maternal Interleukin-6 Is Associated With Macaque Offspring Amygdala Development and Behavior. Cerebral cortex (New York, N.Y. : 1991), 30(3), 1573-1585. https://doi.org/10.1093/cercor/bhz188