Cited by 268Fatty Acid Research and HealthGut microbiota and healthBirth, Development, and Health

Omega-3 polyunsaturated fatty acids critically regulate behaviour and gut microbiota development in adolescence and adulthood

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Robertson, Ruairi C., Seira Oriach, Clara, Murphy, Kiera, Moloney, Gerard M., Cryan, John F., Dinan, Timothy G., Paul Ross, R., Stanton, Catherine·2017·Brain Behavior and Immunity

Abstract

Background Neurodevelopment is strongly influenced by maternal and early-postnatal diet. Omega-3 polyunsaturated fatty acids (n-3 PUFA) are vital structural and functional components of the developing brain. The gut microbiota is also influenced by n-3 PUFA status, however, little is known about the role of maternal and early-life n-3 PUFA intake on offspring gut microbiota development and subsequent interactions with central nervous system functioning and behavioural outcomes.Methods Pregnant female C57BL/6 mice and their male offspring were fed a control (CON), omega-3 deficient (O3-) or omega-3 supplemented (O3+) diet. Cognitive, depressive and social behaviours were assessed through a battery of behaviour tests in the male offspring at both adolescence (week 4-5) and adulthood (week 11-13). Hypothalamic-pituitary-adrenal axis (HPA) activation was assessed by analysis of stress-induced corticosterone production. Fecal microbiota composition was analysed by 16S sequencing at both adolescent and adulthood. In addition, stimulated spleen cytokine levels were assessed.Results n-3 PUFA interventions induced subtle changes in offspring early-life and adolescent behaviours, which were further evident in adulthood, such that O3- animals displayed impaired communication, social and depression-related behaviours and O3+ animals displayed enhanced cognition. O3- mice displayed an elevated Firmicutes:Bacteroidetes ratio and blunted systemic LPS responsiveness. Contrastingly, O3+ mice displayed greater fecal Bifidobacterium and Lactobacillus abundance and dampened HPA-axis activity.Conclusions Neurobehavioural development related to cognitive, anxiety and social behaviours, is highly dependent upon in utero and lifelong n-3 PUFA availability. In addition, neurobehavioural changes induced by altering n-3 PUFA status are closely associated with comprehensive alterations in gut microbiota composition, HPA-axis activity and inflammation.

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Crossref · 10.1016/j.bbi.2016.07.145

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  • In an animal model, specific microbial changes associated with ω-3 fatty acid supplementation were closely related to changes in behavior.

    “Indeed, in an animal model, specific microbial changes (e.g., increased abundance of Lactobacillus and bifidobacteria and altered ratio of bifidobacteria to enterobacteria) associated with ω-3 fatty acid supplementation were closely related to changes in behavior (142).”

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Authors
Robertson, R. C., Seira Oriach, C., Murphy, K., Moloney, G. M., Cryan, J. F., Dinan, T. G., Paul Ross, R., & Stanton, C.
Affiliations
  • Teagasc - The Irish Agriculture and Food Development Authority (IE)
  • University College Cork (IE)
Corresponding author
Stanton, Catherine
Venue
Brain Behavior and Immunity
Publisher
Elsevier BV
Published
2017-01
Volume
59
Pages
21-37
ISSN
0889-1591 (ISSN-L)
OpenAlex
W2462715376
Cited by
268
References
128
Citations by year
2026: 12 · 2025: 25 · 2024: 28 · 2023: 32 · 2022: 35 · 2021: 34 · 2020: 28 · 2019: 32 · 2018: 18 · 2017: 20 · 2016: 4
FWCI
25.74
Type
journal article
Language
en
Open access
Locations
  • Brain Behavior and Immunity (acceptedVersion)
  • PubMed (publishedVersion)
  • Queen Mary Research Online (Queen Mary University of London) (submittedVersion)
Funders
  • Science Foundation Ireland (SFI/12/RC/2273)
  • APC Microbiome Institute
  • Health Research Board of Ireland (HRA_POR/2011/23, HRA_POR/2012/32)
Topics
  • Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords
omega-3 polyunsaturated fatty acids, maternal diet, gut microbiota, brain development, adolescent behavior, social behavior, depression-like behavior, cognitive function, hypothalamic-pituitary-adrenal axis, corticosterone, lipopolysaccharide response, inflammation, Bifidobacterium, Lactobacillus, Firmicutes/Bacteroidetes ratio
MeSH terms
Gastrointestinal Microbiome, Aging, Animals, Behavior, Animal, Cognition, Corticosterone, Depression, Fatty Acids, Fear, Female, Hypothalamo-Hypophyseal System, Male, Mice, Inbred C57BL, Pituitary-Adrenal System, Pregnancy, Social Behavior, Stress, Psychological, Swimming, Vocalization, Animal, Fatty Acids, Omega-3, Cytokines, Recognition, Psychology, Mice

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