Cited by 93Gut microbiota and healthMemory and Neural MechanismsFatty Acid Research and Health

The effect of short-term exposure to energy-matched diets enriched in fat or sugar on memory, gut microbiota and markers of brain inflammation and plasticity

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Beilharz, Jessica E., Kaakoush, Nadeem O., Maniam, Jayanthi, Morris, Margaret J.·2016·Brain Behavior and Immunity

Abstract

Short-term exposure to high-energy diets impairs memory but there is little data on the relative contributions of fat and sugar to these deficits or the mechanisms responsible. Here, we investigated how these different macronutrients affect memory, neuroinflammation and neuroplasticity markers and the gut microbiota. Rats were fed matched purified diets for 2weeks; Control, Sugar, Saturated Fatty Acid (SFA) or Polyunsaturated Fatty Acid (PUFA), which varied only in the percentage of energy available from sugar and the amount and type of fat. Rats consuming SFA and Sugar were impaired on hippocampal-dependent place recognition memory compared to Controls and PUFA rats, despite all rats consuming similar amounts of energy. All rats performed comparably on the object recognition task. Hippocampal and hypothalamic inflammatory markers were not substantially affected by the diets and there was no change in the neuroplasticity marker, brain-derived neurotrophic factor. Each of the diets significantly altered the microbial composition in distinct ways. Specifically, the relative abundance of 89 taxa differed significantly between groups with the majority of these changes accounted for by the Clostridiales order and within that, Lachnospiraceae and Ruminococcaceae. These taxa showed a range of macronutrient specific correlations with place memory. In addition, Distance based Linear Models found relationships between memory, inflammation-related hippocampal genes and the gut microbiota. In conclusion, our study shows that the macronutrient profile of the diet is crucial for diet-induced memory deficits and suggests a possible link between diet, the gut microbiota and hippocampal inflammatory genes.

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Crossref · 10.1016/j.bbi.2016.07.151

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  • Even short-term diet exposure (2 weeks) shifted the microbiota composition in a way that was associated with inflammation-related pathways and memory deficits, indicating rapid effects on microbiota and brain function.

    “Likewise, even short-term diet exposure (2 wk) shifted the microbiota composition in a way that was associated with inflammationrelated pathways and memory deficits (325), indicating rapid effects on microbiota and brain function.”
  • In rats, diets enriched in sugar, SFAs or PUFAs differentially affected the gut microbiota at class, order, family, genus and OTU levels, with 89 taxa contributing to differences among diets.

    “Differential effect of diet at class, order, | family, genus and OTU level; 89 taxa | (16 control; 24 PUFA; 12 SFA; 37 | sugar) contribute to differences | among diets”

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  1. Aggleton, J.P., Brown, M.W., 2005. Contrasting hippocampal and perirhinal cortex function using immediate early gene imaging. The Quarterly journal of experimental psychology. B, Comparative and physiological psychology 58, 218-233.
  2. Takechi, R., Pallebage-Gamarallage, M.M., Lam, V., Giles, C., Mamo, J.C., 2013. Nutraceutical agents with anti-inflammatory properties prevent dietary saturated-fat induced disturbances in blood-brain barrier function in wild-type mice. Journal of neuroinflammation 10, 73.
  3. Wan, H., Aggleton, J.P., Brown, M.W., 1999. Different contributions of the hippocampus and perirhinal cortex to recognition memory. The Journal of neuroscience : the official journal of the Society for Neuroscience 19, 1142-1148.
  4. Zhang, C., Zhang, M., Pang, X., Zhao, Y., Wang, L., Zhao, L., 2012. Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. The ISME journal 6, 1848-1857. Bacterial taxa Actinobacteria.Actinobacteria.Coriobacteriales Actinobacteria.Actinobacteria.Coriobacteriales.Coriobacteriaceae Actinobacteria.Actinobacteria.Coriobacteriales.Coriobacteriaceae.Asaccharobacter.Otu00317 Actinobacteria.Actinobacteria.Coriobacteriales.Coriobacteriaceae.Enterorhabdus.Otu00262 Bacteroidetes.Bacteroidia.Bacteroidales.Bacteroidaceae.Bacteroides.Otu00061 Bacteroidetes.Bacteroidia.Bacteroidales.Porphyromonadaceae.Barnesiella.Otu00043 Bacteroidetes.Bacteroidia.Bacteroidales.Porphyromonadaceae.Barnesiella.Otu00114 Bacteroidetes.Bacteroidia.Bacteroidales.Porphyromonadaceae.Barnesiella.Otu00188 Bacteroidetes.Bacteroidia.Bacteroidales.Porphyromonadaceae.Barnesiella.Otu00252 Bacteroidetes.Bacteroidia.Bacteroidales.Porphyromonadaceae.Barnesiella.Otu00281 Bacteroidetes.Bacteroidia.Bacteroidales.Porphyromonadaceae.Barnesiella.Otu00319 Bacteroidetes.Bacteroidia.Bacteroidales.Porphyromonadaceae.Parabacteroides.Otu00198 Bacteroidetes.Bacteroidia.Bacteroidales.Rikenellaceae Bacteroidetes.Bacteroidia.Bacteroidales.Rikenellaceae.Alistipes Bacteroidetes.Bacteroidia.Bacteroidales.Rikenellaceae.Alistipes.Otu00217 Bacteroidetes.Bacteroidia.Bacteroidales.Rikenellaceae.Alistipes.Otu00470 Bacteroidetes.Bacteroidia.Bacteroidales.unclassified.unclassified.Otu00152 Firmicutes.Bacilli Firmicutes.Bacilli.Lactobacillales Firmicutes.Bacilli.Lactobacillales.Lactobacillaceae Firmicutes.Bacilli.Lactobacillales.Lactobacillaceae.Lactobacillus Firmicutes.Bacilli.Lactobacillales.Lactobacillaceae.Lactobacillus.Otu00002 Firmicutes.Clostridia.Clostridiales.Clostridiaceae_1 Firmicutes.Clostridia.Clostridiales.Clostridiaceae_1.Clostridium_sensu_stricto Firmicutes.Clostridia.Clostridiales.Clostridiaceae_1.Clostridium_sensu_stricto.Otu00022 Firmicutes.Clostridia.Clostridiales.Eubacteriaceae.Eubacterium.Otu00383 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Blautia Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Blautia.Otu00036 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Clostridium_XlVa.Otu00063 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Clostridium_XlVa.Otu00115 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Clostridium_XlVa.Otu00117 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Clostridium_XlVa.Otu00239 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Coprococcus Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Coprococcus.Otu00238 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Marvinbryantia.Otu00375 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Robinsoniella Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.Robinsoniella.Otu00338 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00001 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00015 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00060 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00099 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00104 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00125 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00201 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00232 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00240 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00243 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.Otu00295 Firmicutes.Clostridia.Clostridiales.Lachnospiraceae.unclassified.

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Authors
Beilharz, J. E., Kaakoush, N. O., Maniam, J., & Morris, M. J.
Affiliations
UNSW Sydney (AU)
Corresponding author
Morris, Margaret J.
Venue
Brain Behavior and Immunity
Publisher
Elsevier BV
Published
2016-10
Volume
57
Pages
304-313
ISSN
0889-1591 (ISSN-L)
OpenAlex
W2482754741
Cited by
93
References
45
Citations by year
2026: 4 · 2025: 8 · 2024: 9 · 2023: 7 · 2022: 14 · 2021: 13 · 2020: 14 · 2019: 8 · 2018: 5 · 2017: 10 · 2016: 1
FWCI
4.16
Type
journal article
Language
en
Open access
Locations
  • Brain Behavior and Immunity (publishedVersion)
  • PubMed (publishedVersion)
  • UNSWorks (University of New South Wales, Sydney, Australia) (submittedVersion, cc-by-nc-nd)
  • UNSWorks (UNSW Sydney) (submittedVersion, cc-by-nc-nd)
Funders
  • Medical Research Council
  • National Health and Medical Research Council (1023073)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
Keywords
hypercaloric diet, dietary fat, dietary sugar, memory impairment, hippocampal-dependent memory, gut microbiota, neuroinflammation, neuroplasticity, brain-derived neurotrophic factor, saturated fatty acids, polyunsaturated fatty acids, Clostridiales, Lachnospiraceae, Ruminococcaceae, hypothalamic inflammation, gut-brain axis
MeSH terms
Gastrointestinal Microbiome, Dietary Sugars, Animals, Dietary Fats, Unsaturated, Fatty Acids, Hippocampus, Inflammation, Male, Memory Disorders, Neuronal Plasticity, Biomarkers, Rats, Sprague-Dawley

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