Gut microbiota composition is associated with newborn functional brain connectivity and behavioral temperament

Caroline M Kelsey; Stephanie Prescott; John A McCulloch; Giorgio Trinchieri; Tara L Valladares; Caitlin Dreisbach; Jeanne Alhusen; Tobias Grossmann

doi:10.1016/j.bbi.2020.11.003

Gut microbiota composition is associated with newborn functional brain connectivity and behavioral temperament

Brain Behav Immun. 2021 Jan:91:472-486. doi: 10.1016/j.bbi.2020.11.003. Epub 2020 Nov 4.

Authors

Caroline M Kelsey¹, Stephanie Prescott², John A McCulloch³, Giorgio Trinchieri³, Tara L Valladares⁴, Caitlin Dreisbach⁵, Jeanne Alhusen⁶, Tobias Grossmann⁷

Affiliations

¹ Department of Psychology, University of Virginia, Charlottesville, VA, USA; Department of Pediatrics, Division of Developmental Medicine, Boston Children's Hospital, Boston, MA, USA; Harvard Medical School, MA, USA. Electronic address: C.Kelsey@virginia.edu.
² National Cancer Institute, National Institutes of Health, Bethesda, MD, USA; College of Nursing, University of South Florida, Tampa, FL, USA.
³ National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
⁴ Department of Psychology, University of Virginia, Charlottesville, VA, USA.
⁵ School of Nursing, University of Virginia, Charlottesville, VA, USA; Data Science Institute, Columbia University, NY, USA.
⁶ School of Nursing, University of Virginia, Charlottesville, VA, USA.
⁷ Department of Psychology, University of Virginia, Charlottesville, VA, USA; Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany. Electronic address: Grossmann@virginia.edu.

PMID: 33157257
DOI: 10.1016/j.bbi.2020.11.003

Abstract

The gut microbiome appears to play an important role in human health and disease. However, only little is known about how variability in the gut microbiome contributes to individual differences during early and sensitive stages of brain and behavioral development. The current study examined the link between gut microbiome, brain, and behavior in newborn infants (N = 63; M [age] = 25 days). Infant gut microbiome diversity was measured from stool samples using metagenomic sequencing, infant functional brain network connectivity was assessed using a resting state functional near infrared spectroscopy (rs-fNIRS) procedure, and infant behavioral temperament was assessed using parental report. Our results show that gut microbiota composition is linked to individual variability in brain network connectivity, which in turn mediated individual differences in behavioral temperament, specifically negative emotionality, among infants. Furthermore, virulence factors, possibly indexing pathogenic activity, were associated with differences in brain network connectivity linked to negative emotionality. These findings provide novel insights into the early developmental origins of the gut microbiome-brain axis and its association with variability in important behavioral traits. This suggests that the gut microbiome is an important biological factor to consider when studying human development and health.

Keywords: Default mode network; Fronto-parietal network; Functional connectivity; Homologous-interhemispheric network; Temperament; fNIRS.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Adult
Brain
Gastrointestinal Microbiome*
Humans
Infant
Infant, Newborn
Temperament