Gut microbiota composition is associated with newborn functional brain connectivity and behavioral temperament
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.
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Using one pipeline to reanalyze shotgun data largely reproduced prior taxonomic differences between responders and nonresponders, but datasets overlapped little.
“Reanalysis of the shotgun datasets using the same bioinformatics pipeline11,34,35 mostly reproduced reported taxonomic differences between Rs and NRs with minimal overlap between datasets (Supplementary Fig. 7a–d).”
From Intestinal microbiota signatures of clinical response and immune-related adverse events in melanoma patients treated with anti-PD-1 (2022) · cites this paper as [35]
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Kelsey, C. M., Dreisbach, C., Alhusen, J. L., & Großmann, T. (2018) · Developmental Psychobiology · doi:10.1002/dev.21778 · Cited by 20 · see citing works
Self-citationRigato, S., Stets, M., Bonneville‐Roussy, A., & Holmboe, K. (2020) · Social Development · doi:10.1111/sode.12448 · Cited by 20 · see citing works
Infants’ brain responses to pupillary changes in others are affected by race
Kelsey, C. M., Krol, K. M., Kret, M. E., & Großmann, T. (2019) · Scientific Reports · doi:10.1038/s41598-019-40661-z · Cited by 19 · see citing works
Self-citationA call for mapping the development of the microbiota-gut-brain axis during human infancy
Kelsey, C. M., & Großmann, T. (2019) · Behavioral and Brain Sciences · doi:10.1017/s0140525x18002923 · Cited by 4 · see citing works
Self-citationAatsinki, A., Lahti, L., Munukka, E., Keskitalo, A., Karlsson, H., & Karlsson, L. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.07.006 · Cited by 4 · see citing works
Homologous Connectivity Maps Can Discriminate Diseased from Healthy Brains
Patashov, D., Goldstein, D., & Balberg, M. (2019) · doi:10.1364/brain.2019.bw4a.3 · Cited by 3 · see citing works
Kelsey, C. M., Farris, K., & Großmann, T. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.15.204271 · Cited by 3 · see citing works
Self-citation
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McCulloch, J. A., Davar, D., Rodrigues, R. R., Badger, J. H., Fang, J. R., Cole, A. M., Balaji, A. K., Vetizou, M., Prescott, S. M., Fernandes, M. R., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-01698-2 · Cited by 472 · see citing works
Self-citationSpichak, S., Bastiaanssen, T. F. S., Berding, K., Vlckova, K., Clarke, G., Dinan, T. G., & Cryan, J. F. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.044 · Cited by 127 · see citing works
- Authors
- Kelsey, C. M., Prescott, S., McCulloch, J. A., Trinchieri, G., Valladares, T. L., Dreisbach, C., Alhusen, J., & Grossmann, T.
- Affiliations
- Boston Children's Hospital (US)
- National Institutes of Health (US)
- University of Virginia (US)
- Max Planck Institute for Human Cognitive and Brain Sciences (DE)
- Corresponding author
- Kelsey, Caroline M.
- Grossmann, Tobias
- ORCID
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2021-01
- Volume
- 91
- Pages
- 472-486
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W3095276920
- Cited by
- 116
- References
- 101
- Citations by year
- 2026: 10 · 2025: 24 · 2024: 31 · 2023: 19 · 2022: 24 · 2021: 8
- FWCI
- 4.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- University of Virginia
- National Science Foundation (2017229, 1842490)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Health Professions › Pharmacy › Infant Health and Development
- Keywords
- gut microbiota, gut-brain axis, neonates, brain functional connectivity, resting-state fNIRS, negative affectivity, microbial virulence factors, microbiome diversity, individual differences, early brain development
- MeSH terms
- Gastrointestinal Microbiome, Adult, Brain, Humans, Infant, Infant, Newborn, Temperament
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