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Omega-3 polyunsaturated fatty acids critically regulate behaviour and gut microbiota development in adolescence and adulthood
Open accessAbstract
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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“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).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [142]
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Metadata
- 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
- ORCID
- 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
- FWCI
- 25.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (am, 341 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- 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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