Nucleus accumbens inflammation mediates anxiodepressive behavior and compulsive sucrose seeking elicited by saturated dietary fat
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OBJECTIVE: The incidence of depression is significantly compounded by obesity. Obesity arising from excessive intake of high-fat food provokes anxiodepressive behavior and elicits molecular adaptations in the nucleus accumbens (NAc), a region well-implicated in the hedonic deficits associated with depression and in the control of food-motivated behavior. To determine the etiology of diet-induced depression, we studied the impact of different dietary lipids on anxiodepressive behavior and metabolic and immune outcomes and the contribution of NAc immune activity. METHODS: Adult C57Bl/6 mice were subjected to isocaloric high-fat/high-sucrose diets (HFD), enriched in either saturated or monounsaturated fat, or a control low-fat diet (LFD). Metabolic responses, anxiodepressive behavior, and plasma and NAc inflammatory markers were assessed after 12 weeks. In separate experiments, an adenoviral construct inhibiting IKKβ, an upstream component of the nuclear factor kappa-b (NFkB) pathway, was a priori injected into the NAc. RESULTS: Both HFDs resulted in obesity and hyperleptinemia; however, the saturated HFD uniquely triggered anxiety-like behavior, behavioral despair, hyperinsulinemia, glucose intolerance, peripheral inflammation, and multiple pro-inflammatory signs in the NAc, including reactive gliosis, increased expression of cytokines, antigen-presenting markers and NFкB transcriptional activity. Selective NAc IKKβ inhibition reversed the upregulated expression of inflammatory markers, prevented anxiodepressive behavior and blunted compulsive sucrose-seeking in mice fed the saturated HFD. CONCLUSIONS: Metabolic inflammation and NFкB-mediated neuroinflammatory responses in the NAc contribute to the expression of anxiodepressive behavior and heightened food cravings caused by a diet high in saturated fat and sugar.
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Oleate can improve glycemic control and plasma lipid profiles in humans and protect against inflammation, hyperphagia, and anxiodepressive behaviors in mice.
“Oleate, a monounsaturated fatty acid enriched in olive oil, can improve glycemic control and plasma lipid profiles in humans and protect against inflammation, hyperphagia, and anxiodepressive behaviors in mice [34,42].”
From The menace of obesity to depression and anxiety prevalence (2022) · cites this paper as [34]
Viral inhibition of IKK and NF-κB in NAc prevents neuroinflammation and forced-swim immobility caused by high-fat diet.
“Viral inhibition of IKK and NF-κB in NAc also prevents neuroinflammation and forced-swim immobility caused by high-fat diet [190].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [190]
Anhedonia caused by high-fat diet or restraint stress is associated with increased ionized calcium-binding adaptor molecule 1-positive microglia in several brain regions including the NAc.
“Anhedonia caused by high-fat diet or restraint stress is associated with increased ionized calcium-binding adaptor molecule 1-positive microglia in several brain regions including the NAc [189, 190].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [190]
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Nucleus accumbens cytoarchitecture predicts weight gain in children
Rapuano, K. M., Laurent, J. S., Hagler, D. J., Hatton, S. N., Thompson, W. K., Jernigan, T. L., Dale, A. M., Casey, B. J., & Watts, R. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2007918117 · Cited by 79 · see citing works
Brain control of energy homeostasis: implications for anti-obesity pharmacotherapy
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Demers, G., Roy, J., Machuca-Parra, A. I., Dashtehei pour, Z., Bairamian, D., Daneault, C., Rosiers, C. D., Ferreira, G., Alquier, T., Fulton, S., et al. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-0623-6 · Cited by 53 · see citing works
Lin, M.-H., Cheng, P.-C., Hsiao, P.-J., Chen, S.-C., Hung, C.-H., Kuo, C.-H., Huang, S.-K., & Clair Chiou, H.-Y. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109653 · Cited by 42 · see citing works
GLP-1/dexamethasone inhibits food reward without inducing mood and memory deficits in mice
Décarie-Spain, L., Fisette, A., Zhu, Z., Yang, B., DiMarchi, R. D., Tschöp, M. H., Finan, B., Fulton, S., & Clemmensen, C. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.03.035 · Cited by 27 · see citing works
Self-citationNeuronal nitric oxide synthase regulates depression-like behaviors in shortening-induced obese mice
Wang, P., Kong, F.-Z., Hong, X.-H., Zhang, L., Zhao, W.-H., Yang, J.-C., & Zhang, H. (2022) · Nutrients · doi:10.3390/nu14204302 · Cited by 11 · see citing works
- Authors
- Décarie-Spain, L., Sharma, S., Hryhorczuk, C., Issa-Garcia, V., Barker, P. A., Arbour, N., Alquier, T., & Fulton, S.
- Affiliations
- Centre Hospitalier de l’Université de Montréal (CA)
- University of British Columbia (CA)
- Corresponding author
- Fulton, Stephanie
- ORCID
- Venue
- Molecular Metabolism
- Publisher
- Elsevier BV
- Published
- 2018-04
- Volume
- 10
- Pages
- 1-13
- ISSN
- 2212-8778 (ISSN-L)
- PMC
- PMC5985233
- OpenAlex
- W2792728053
- Cited by
- 107
- References
- 80
- Citations by year
- 2026: 10 · 2025: 10 · 2024: 14 · 2023: 13 · 2022: 16 · 2021: 18 · 2020: 11 · 2019: 9 · 2018: 6
- FWCI
- 3.50
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Molecular Metabolism (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- CIHR
- FRQS
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- nucleus accumbens, neuroinflammation, saturated fat, high-fat diet, obesity, NF-κB signaling, IKKβ inhibition, reactive gliosis, hyperleptinemia, hyperinsulinemia, impaired glucose tolerance, peripheral inflammation, food cravings
- MeSH terms
- Food Addiction, Animals, Anxiety Disorders, Depressive Disorder, Inflammation, Male, Mice, Inbred C57BL, Nucleus Accumbens, Dietary Sucrose, Mice, I-kappa B Kinase, Diet, High-Fat
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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