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Diets containing long-chain n-3 polyunsaturated fatty acids affect behaviour differently during development than ageing in mice

Published online by Cambridge University Press:  09 March 2007

Isabelle Carrié*
Affiliation:
INSERM U. 26, Unité de Neuro-Pharmaco-Nutrition, Hôpital. F. Widal, 200 rue du Faubourg St Denis, 75010 Paris, France
Philippe Guesnet
Affiliation:
INRA, Laboratoire de Sécurité Alimentaire, 78352 Jouy en Josas, France
Jean-Marie Bourre
Affiliation:
INSERM U. 26, Unité de Neuro-Pharmaco-Nutrition, Hôpital. F. Widal, 200 rue du Faubourg St Denis, 75010 Paris, France
Henriette Francès
Affiliation:
INSERM U. 26, Unité de Neuro-Pharmaco-Nutrition, Hôpital. F. Widal, 200 rue du Faubourg St Denis, 75010 Paris, France
*
*Corresponding author: Dr Isabelle Carrié, fax +33 (1) 40 34 40 64, email [email protected]
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Abstract

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The effect of a standard diet providing essential fatty acids enriched in fish oil or palm oil was studied in young, mature and old mice. Two groups of pregnant and lactating OF1 mice were fed on diets with or without high levels of long-chain n-3 polyunsaturated fatty acids. Offspring were maintained on these diets after weaning. The litter size did not differ. The weight increased more quickly in fish-oil-fed mice than palm-oil-fed mice. The fish-oil diet induced a significant increase in exploratory activity in young mice which was not found in mature and old mice. The level of locomotor activity was significantly higher in young, no different in mature, and lower in old fish-oil-fed mice than in controls. Habituation, the simpler form of learning, occurred to the same extent in the two diet groups. For the place learning protocol of the Morris water maze there was no difference between the two diet groups; however, in the probe trial, the mature fish-oil-fed mice remembered the situation well compared with the control mice. In the active avoidance test, on the first day of acquisition the young fish-oil-fed mice made more avoidances than control mice, whereas in contrast, mature and old-fish-fed mice made less avoidances than control mice. These results suggest a positive effect on arousal and learning ability of a diet enriched in long chain n-3 polyunsaturated fatty acids in young mice and a detrimental effect in old mice.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Bourre, JMFrançois, M, Youyou, A, Dumont, O, Piciotti, M, Pascal, G and Durand, G (1989) The effects of dietary α-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. Journal of Nutrition 119, 18801892.CrossRefGoogle ScholarPubMed
Brandeis, R, Brandys, Y and Yehuda, S (1989) The use of Morris Water Maze in the study of memory and learning. International Journal of Neuroscience 48, 2969.CrossRefGoogle Scholar
Carrié, I, Debray, M, Bourre, JM and Francès, H (1999) Age-induced cognitive alterations in OF1 mice. Physiology and Behavior 66, 651656.CrossRefGoogle ScholarPubMed
Connor, WE, Neuringer, M and Reisbick, S (1992) Essential fatty acids: the importance of. n-3 fatty acids in the retina and brain. Nutrition Reviews 50, 2129.CrossRefGoogle ScholarPubMed
Coscina, DV (1997) Polyunsaturated fats and learning, old data, new questions. In Handbook of Essential Fatty Acid Biology, pp. 215244 [Yehuda, S, and Mostofsky, DI, editors]. Totowa, NJ, Humana Press.CrossRefGoogle Scholar
Coscina, DV, Yehuda, S, Dixon, LM, Kish, SJ and Leprohon-Greenwood, CE (1986) Learning is improved by a soybean oil diet in rats. Life Sciences 38, 17891794.CrossRefGoogle ScholarPubMed
Enslen, M, Milon, H and Malnoe, A (1991) Effect of low intake of (n-3) fatty acids during development on brain phospholipids, fatty acid composition and exploratory behaviour in rats. Lipids 26, 203208.CrossRefGoogle ScholarPubMed
Foreman-van Drongelen, Mvan Houwelingen, A, Kester, A, Blanco, C, Hasaart, T and Hornstra, G (1996) Influence of feeding artificial-formula milks containing docosahexaenoic and arachidonic acids on the postnatal long-chain polyunsaturated fatty acid status of healthy preterm infants. British Journal of Nutrition 76, 649667.CrossRefGoogle ScholarPubMed
Francès, H, Monier, CClément, M, Lecorsier, A, Debray, M and Bourre, JM (1996) Effect of dietary alpha-linolenic acid deficiency on habituation. Life Science 58, 18051816.CrossRefGoogle ScholarPubMed
Galli, C, Messeri, GP, Oliverio, A and Paoletti, R (1975) Deficiency of essential fatty acids during pregnancy and avoidance learning in the progeny. Pharmacological Research Communications 7, 7180.CrossRefGoogle Scholar
Gallagher, M and Pelleymounter, MA (1988) Spatial learning deficits in old rats: a model for memory declined in the aged. Neurobiology of Ageing 9, 549556.CrossRefGoogle Scholar
Garrido, A and Lopez, C (1998) Lipoprotein lipase activity and protein oxidative damage are increased in brain by age but not by fish oil ingestion. Nutrition Research 18, 519531.CrossRefGoogle Scholar
Ide, T, Murata, M and Sugano, M (1996) Stimulation of the activities of hepatic fatty acid oxidation enzymes by dietary fat rich in α-linolenic acid in rats. Journal of Lipid Research 37, 448463.CrossRefGoogle Scholar
Jensen, MM, Skarsfeld, T and Hoy, CE (1996) Correlation between level of (n-3) polyunsaturated fatty acids in brain phospholipids and learning ability in rats. A multiple generation study. Biochimica et Biophysica Acta 1300, 203209.CrossRefGoogle ScholarPubMed
Kalmijn, S, Feskens, EJM, Launer, LJ and Kromhout, D (1997) Polyunsaturated fatty acids, antioxidants, and cognitive function in very old men. American Journal of Epidemiology 145, 3341.CrossRefGoogle ScholarPubMed
Lamberty, Y and Gower, AJ (1991) Simplifying environmental cues in the Morris-type water maze improves place learning in old NMRI mice. Behavioral Neural Biology 56, 89100.CrossRefGoogle ScholarPubMed
Lamptey, MS and Walker, BL (1976) A possible essential role for dietary linolenic acid in the development of young rat. Journal of Nutrition 106, 8693.CrossRefGoogle ScholarPubMed
Lucas, A (1997) Long-chain polyunsaturated fatty acids, infant feeding and cognitive development. In Developing Brain and Behaviour; The Role of Lipids in Infant Formula, pp. 339 [Dobbing, J, editor]. London: Academic Press.CrossRefGoogle Scholar
Mills, DE, Ward, RP and Young, C (1988) Effects of prenatal and early postnatal fatty acid supplementation on behavior. Nutrition Research 8, 273286.CrossRefGoogle Scholar
Miyamoto, M, Kiyota, Y, Yamazaki, N, Nagaoka, A, Matsuo, T, Nagawa, Y and Takeda, T (1986) Age-related changes in learning and memory in the senescence-accelerated mouse (SAM). Physiology and Behavior 38, 399406.CrossRefGoogle ScholarPubMed
Nakashima, Y, Yuasa, S, Hakamizu, Y, Okuyama, H, Ohhara, T, Kameyama, T and Nabeshima, T (1993) Effect of a high linoleate and a high alpha-linolenate diet on general behavior and drug sensitivity in mice. Journal of Lipid Research 34, 239247.CrossRefGoogle Scholar
Sen, CK, Atalay, M, Agren, J, Laaksonen, DE, Roy, S and Hanninen, O (1997) Fish oil and vitamin E supplementation in oxidative stress at rest and after physical exercise. Journal of Applied Physiology 83, 189195.CrossRefGoogle ScholarPubMed
Stavnes, K and Sprott, RL (1975) Effects of age and genotype on acquisition of an active avoidance response in mice. Developmental Psychobiology 8, 437445.CrossRefGoogle ScholarPubMed
Suzuki, H, Park, SJ, Tamura, M and Ando, S (1998) Effect of long-term feeding of dietary lipids on the learning ability, fatty acid composition of brain stem phospholipids and synaptic membrane fluidity in adult mice: a comparison of sardine oil diet with palm oil diet. Mechanisms of Ageing and Development 101, 119128.CrossRefGoogle ScholarPubMed
Umezawa, M, Ohta, A, Tojo, H, Yagi, H, Hosokawa, M and Takeda, T (1995) Dietary α-linolenate/linoleate balance influences learning and memory in the senescence-accelerated mouse (SAM). Brain Research 669, 225233.CrossRefGoogle ScholarPubMed
Wainwright, PE, Huang, YS, Coscina, DV, Levesque, S and McCutcheon D (1994) Brain and behavioural effects of dietary (n-3) deficiency in mice: a three generational study. Developmental Psychobiology 27, 467487.CrossRefGoogle ScholarPubMed
Wainwright, PE, Xing, HC, Mutsaers, LMcCutcheon, D and Kyle, D (1997) Arachidonic acid offsets the effects on mouse brain and behavior of a diet with a low (n-6) : (n-3) ratio and very high levels of docosahexaenoic acid. Journal of Nutrition 127, 184193.CrossRefGoogle Scholar
Weisinger, HS, Vingrys, AJ and Sinclair, AJ (1996) The effect of docosahexaenoic acid on the electroretinogram of the guinea pig. Lipids 31, 6570.CrossRefGoogle ScholarPubMed
Wilcock, J and Broadhurst, PJ (1967) Strain differences in emotionality: open-field and conditioned avoidance behaviour in the rat. Journal of Comparative and Physiological Psychology 63, 335338.CrossRefGoogle ScholarPubMed
Yamamoto, N, Hashimoto, A, Takemoto, Y, Okuyama, H, Nomura, M, Kitajima, R, Togashi, T and Tamai, Y (1988) Effect of the dietary α-linolenate/linoleate balance on lipid compositions and learning ability of rats. II. Discrimination process, extinction process, and glycolipid compositions. Journal of Lipid Research 29, 10131021.CrossRefGoogle ScholarPubMed
Yamamoto, N, Okaniwa, Y, Mori, S, Nomura, M and Okuyama, H (1991) Effects of a high-linoleate and a high-α-linolenate diet on the learning ability of aged rats. Journal of Gerontology 46, B17B22.CrossRefGoogle Scholar
Yamamoto, N, Saitoh, M, Moriuchi, A, Nomura, M and Okuyama, H (1987) Effect of dietary α-linolenate/linoleate balance on brain lipid compositions and learning ability of rats. Journal of Lipid Research 28, 144151.CrossRefGoogle ScholarPubMed
Yehuda, S and Carasso, RL (1993) Modulation of learning, pain thresholds, and thermoregulation in the rat by preparations of free purified alpha-linolenic and linoleic acids: determination of the optimals ω3-to-ω6 ratio. Proceedings of the National Academy of Sciences USA 90, 1034510349.CrossRefGoogle Scholar
Yonekubo, A, Honda, S, Okano, M, Takahashi, K and Yamamoto, Y (1994) Effects of dietary fish oil during the fetal and postnatal periods on the learning ability of postnatal rats. Bioscience Biotechnology and Biochemistry 58, 799801.CrossRefGoogle Scholar
Yonekubo, A, Honda, S, Okano, M and Yamamoto, Y (1993) Effects of dietary safflower oil or soybean oil on the milk composition of the maternal rat, and tissue fatty acid composition and learning ability of postnatal rats. Bioscience Biotechnology and Biochemistry 57, 253259.CrossRefGoogle ScholarPubMed