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Article

Dietary Long-Chain n-3 Polyunsaturated Fatty Acid Supplementation Alters Electrophysiological Properties in the Nucleus Accumbens and Emotional Behavior in Naïve and Chronically Stressed Mice

1
Laboratoire NutriNeuro, UMR INRAE 1286, Bordeaux INP, Université de Bordeaux, 146 Rue Léo Saignat, 33076 Bordeaux, France
2
Worcester Biomedical Research Group, School of Science and the Environment, University of Worcester, Worcester WR2 6AJ, UK
3
International Research Network Food4BrainHealth
4
Department of Clinical Nutrition, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah 22254, Saudi Arabia
5
Department of Nutritional Sciences, Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A1, Canada
*
Author to whom correspondence should be addressed.
Academic Editors: Jérôme Roy and Nobuyuki Takahashi
Int. J. Mol. Sci. 2022, 23(12), 6650; https://doi.org/10.3390/ijms23126650
Received: 12 May 2022 / Revised: 8 June 2022 / Accepted: 13 June 2022 / Published: 14 June 2022
(This article belongs to the Special Issue Nutrition and Metabolism in Health and Disease: From Gene to Organism)
Long-chain (LC) n-3 polyunsaturated fatty acids (PUFAs) have drawn attention in the field of neuropsychiatric disorders, in particular depression. However, whether dietary supplementation with LC n-3 PUFA protects from the development of mood disorders is still a matter of debate. In the present study, we studied the effect of a two-month exposure to isocaloric diets containing n-3 PUFAs in the form of relatively short-chain (SC) (6% of rapeseed oil, enriched in α-linolenic acid (ALA)) or LC (6% of tuna oil, enriched in eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA)) PUFAs on behavior and synaptic plasticity of mice submitted or not to a chronic social defeat stress (CSDS), previously reported to alter emotional and social behavior, as well as synaptic plasticity in the nucleus accumbens (NAc). First, fatty acid content and lipid metabolism gene expression were measured in the NAc of mice fed a SC (control) or LC n-3 (supplemented) PUFA diet. Our results indicate that LC n-3 supplementation significantly increased some n-3 PUFAs, while decreasing some n-6 PUFAs. Then, in another cohort, control and n-3 PUFA-supplemented mice were subjected to CSDS, and social and emotional behaviors were assessed, together with long-term depression plasticity in accumbal medium spiny neurons. Overall, mice fed with n-3 PUFA supplementation displayed an emotional behavior profile and electrophysiological properties of medium spiny neurons which was distinct from the ones displayed by mice fed with the control diet, and this, independently of CSDS. Using the social interaction index to discriminate resilient and susceptible mice in the CSDS groups, n-3 supplementation promoted resiliency. Altogether, our results pinpoint that exposure to a diet rich in LC n-3 PUFA, as compared to a diet rich in SC n-3 PUFA, influences the NAc fatty acid profile. In addition, electrophysiological properties and emotional behavior were altered in LC n-3 PUFA mice, independently of CSDS. Our results bring new insights about the effect of LC n-3 PUFA on emotional behavior and synaptic plasticity. View Full-Text
Keywords: DHA; EPA; ALA; chronic social defeat stress; lipid microarray; whole-cell patch-clamp electrophysiology; long-term depression; emotional behavior DHA; EPA; ALA; chronic social defeat stress; lipid microarray; whole-cell patch-clamp electrophysiology; long-term depression; emotional behavior
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MDPI and ACS Style

Di Miceli, M.; Martinat, M.; Rossitto, M.; Aubert, A.; Alashmali, S.; Bosch-Bouju, C.; Fioramonti, X.; Joffre, C.; Bazinet, R.P.; Layé, S. Dietary Long-Chain n-3 Polyunsaturated Fatty Acid Supplementation Alters Electrophysiological Properties in the Nucleus Accumbens and Emotional Behavior in Naïve and Chronically Stressed Mice. Int. J. Mol. Sci. 2022, 23, 6650. https://doi.org/10.3390/ijms23126650

AMA Style

Di Miceli M, Martinat M, Rossitto M, Aubert A, Alashmali S, Bosch-Bouju C, Fioramonti X, Joffre C, Bazinet RP, Layé S. Dietary Long-Chain n-3 Polyunsaturated Fatty Acid Supplementation Alters Electrophysiological Properties in the Nucleus Accumbens and Emotional Behavior in Naïve and Chronically Stressed Mice. International Journal of Molecular Sciences. 2022; 23(12):6650. https://doi.org/10.3390/ijms23126650

Chicago/Turabian Style

Di Miceli, Mathieu, Maud Martinat, Moïra Rossitto, Agnès Aubert, Shoug Alashmali, Clémentine Bosch-Bouju, Xavier Fioramonti, Corinne Joffre, Richard P. Bazinet, and Sophie Layé. 2022. "Dietary Long-Chain n-3 Polyunsaturated Fatty Acid Supplementation Alters Electrophysiological Properties in the Nucleus Accumbens and Emotional Behavior in Naïve and Chronically Stressed Mice" International Journal of Molecular Sciences 23, no. 12: 6650. https://doi.org/10.3390/ijms23126650

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