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Distribution, depletion and recovery of docosahexaenoic acid are region-specific in rat brain

Published online by Cambridge University Press:  08 March 2007

Ying Xiao
Affiliation:
Food and Nutritional Sciences Programme, Department of Biochemistry, The Chinese University of Hong Kong, Shatin, NT, Hong Kong, China Department of Nutrition and Food Hygiene, University Health Science Center, Peking University, Beijing, China
Yu Huang
Affiliation:
Department of Physiology, The Chinese University of Hong Kong, Shatin, NT, Hong Kong, China
Zhen-Yu Chen*
Affiliation:
Food and Nutritional Sciences Programme, Department of Biochemistry, The Chinese University of Hong Kong, Shatin, NT, Hong Kong, China
*
*Corresponding author: Dr Zhen-Yu Chen, fax +852 2603 7246, email zhenyuchen@cuhk.edu.hk
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Abstract

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The present study examined: (i) age-induced regional changes in fatty acid composition of brain phospholipids; (ii) α-linolenic acid deficiency-induced regional depletion and recovery of DHA in the brain. DHA and arachidonic acid (AA) did not distribute evenly in the brain. In weaning and adult rats, the region with the highest DHA percentage was the cortex whereas the medulla had the lowest DHA percentage. In the aged rats, both the cortex and cerebellum were the regions with the highest DHA percentage whereas in the neonatal rats, the striatum had the greatest percentage of DHA, and the hypothalamus and hippocampus had the least percentage of DHA. Regarding AA, the hippocampus was the region that had the highest percentage whereas the medulla was the region with the lowest percentage except for the neonatal rats, whose cerebellum, hypothalamus, striatum and midbrain had AA percentage lower than hippocampus and cortex. DHA was not proportionally depleted in various regions of brain when the rats were maintained on an n-3-deficient diet for two generations. The results demonstrated that the cortex, hippocampus, striatum, cerebellum and hypothalamus had DHA depleted by >71 %, whereas the midbrain and medulla had only 64 and 57 % DHA depleted, respectively. The most important observation was that the diet reversal for 12 weeks resulted in complete DHA recovery in all regions except for the medulla where the recovery was only 62 %. It was concluded that the location of DHA, n-3 deficiency-induced DHA depletion and reversibility of DHA deficiency across the brain were region-specific.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2005

References

Agostoni, C, Trojan, S, Bellu, R, Riva, D & Giovannini, M (1995) Neurodevelopment quotient of healthy term infants at 4 months and feeding practice: the role of long-chain polyunsaturated fatty acids. Pediatr Res 38, 262266.CrossRefGoogle Scholar
Auestad, N, Montalto, MB, Hall, RT, Fitzgerald, KM, Wheeler, RE, Connor, WE, Neuringer, M, Connor, SL, Taylor, JA & Hartmann, EE (1997) Visual acuity, erythrocyte fatty acid composition, and growth in term infants fed formulas with long chain polyunsaturated fatty acids for one year. Ross Pediatric Lipid Study. Pediatr Res 41, 110.CrossRefGoogle ScholarPubMed
Bennett, TL (1977)The anatomy of the brain. In Brain and Behavior, 2450. Monterey, CA: Brooks/Cole Publishing Company.Google Scholar
Birch, EE, Garfield, S, Hoffman, DR, Uauy, R & Birch, DG (2000) A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants. Dev Med Child Neurol 42, 174181.Google ScholarPubMed
Bourre, JM, Francois, M, Youyou, A, Dummont, D, Piciotti, M, Pascal, G & Durand, G (1989) The effects of dietary alpha-linolenic acid on the composition of nerve membrane, enzymatic activity, amplitude of electrophysiological parameters, resistance to poison and performance of learning tasks in rats. J Nutr 119, 18801892.CrossRefGoogle ScholarPubMed
Carlson, SE & Werkman, SH (1996) A randomized trial of visual attention of perterm infants fed docosahexaenoic acid until two months. Lipids 31, 8590.CrossRefGoogle Scholar
Carlson, SE, Werkman, SH, Rhodes, PG & Tolley, EA (1993) Visual-acuity development in healthy preterm infants; effect of marine-oil supplementation. Am J Clin Nutr 58, 3542.CrossRefGoogle ScholarPubMed
Carrie, I, Clement, M, de Javel, D, Fances, H & Bourre, JM (2000) Specific phospholipid fatty acid composition of brain regions in mice: effect of n -3 polyunsturated fatty acid deficiency and phospholipid supplementationM. J Lipid Res 41, 465472.CrossRefGoogle Scholar
Connor, WE, Neuringer, M & Lin, DS (1990) Dietary effect on brain fatty acid composition: the reversibility of n -3 fatty acid deficiency and turnover of docosahexaneoic acid in the brain, erythrocytes, and plasma of rhesus monkeys. J Lipid Res 31, 237247.CrossRefGoogle Scholar
Enslen, M, Milon, H & Malnoe, A (1991) Effect of low intake of n -3 fatty acids during development on brain phospholipids fatty acid composition and exploratory behavior in rats. Lipids 26 203208.CrossRefGoogle Scholar
Favreliere, S, Barruer, L, Durand, G, Chalon, S & Tallibeay, C (1998) Chronic dietary n -3 deficiency affects the fatty acid composition of plasmenylethanolamine and phosphatidylethanolamine differently in rat frontal cortex, striatum and cerebellum. Lipids 33, 401407.CrossRefGoogle ScholarPubMed
Glowinski, J & Iversen, LL (1966) Regional studies of catecholamines in the rat brain. I. The disposition of [3 H]norepinephrine, [3 H]dopamine and [3 H]DOPA in various regions of the brain. J Neurochem 13, 655669.CrossRefGoogle Scholar
Greiner, RS, Moriguchi, T, Hutton, A, Slotnick, BM & Salem, N (1999) Rats with low level of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids 34, S239S243.CrossRefGoogle ScholarPubMed
Innis, SM (2004) Polyunsaturated fatty acids in human milk: an essential role in infant development. Ad Exp Med Biol 554, 2743.CrossRefGoogle ScholarPubMed
Innis, SM, Nelson, CM, Rioux, MF & King, DJ (1994) Development of visual acuity in relation to plasma and erythrocyte omega-6 and omega-3 fatty acids in healthy term gestation infants. Am J Clin Nutr 60, 347352.CrossRefGoogle ScholarPubMed
Jorgensen, MH, Holmer, G, Lund, P, Hernell, O & Michaelsen, KF (1998) Effect of formula supplemented with docosahexaenoic acid and gamma-linolenic acid on fatty acid status and visual acuity in term infants. J Pediatr Gastroenterol Nutr 26, 412421.Google Scholar
Lamptey, MS & Walker, BL (1976) A possible essential role for dietary linolenic acid in the development of the young rat. J Nutr 106, 8693.CrossRefGoogle ScholarPubMed
Lim, SY & Suzuki, H (2001) Changes in maze behavior of mice occur after sufficient accumulation of docosahexaenoic acid in brain. J Nutr 131, 319324.CrossRefGoogle ScholarPubMed
Lucas, A, Morley, R, Stephenson, T & Elias-Jones, A (2002) Long-chain polyunsaturated fatty acids and infant formula [Letter]. Lancet 360, 1178.CrossRefGoogle ScholarPubMed
Lucas, A, Stafford, M, Morley, R, Abbott, R, Stephenson, T, MacFadyen, U & Elias-Jones, A (1999) Efficacy and safety of long-chain polyunsaturated fatty acid supplementation of infant-formula milk: a randomized trial. Lancet 354, 19481954.CrossRefGoogle Scholar
Makrides, M, Neumann, MA, Simmer, K & Gibson, R (1995) Are long-chain polyunsaturated fatty acids essential nutrients in infancy?. Lancet 345, 14631468.CrossRefGoogle ScholarPubMed
Marteinsdottir, I, Horrobin, DF, Stenfors, C, Theodorsson, E & Mathe, AA (1998) Changes in dietary fatty acids alter phospholipid fatty acid composition in selected regions of rat brain. Prog Neuropsychopharmacol Biol Psychiatry 22, 10071021.CrossRefGoogle ScholarPubMed
Moriguchi, T, Greiner, RS & Salem, N (2000) Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J Neurochem 75, 25632573.CrossRefGoogle ScholarPubMed
Moriguchi, T, Loewke, J, Garrison, M, Catalan, JN & Salem, N (2001) Reversal of docosahexaenoic acid deficiency in the rat brain, retina, liver and serum. J Lipid Res 42, 419427.CrossRefGoogle ScholarPubMed
Moriguchi, T & Salem, N (2003) Recovery of brain docosahexaneoate leads to recovery of spatial task performance. J Neurochem 87, 297309.CrossRefGoogle ScholarPubMed
Neuringer, MW, Connor, E, Lin, DS, Barstad, L & Luck, S (1986) Biochemical and functional effects of prenatal and postnatal omega 3 fatty acid deficiency on retina and brain in rhesus monkeys. Proc Natl Acad Sci USA 83, 40214025.CrossRefGoogle ScholarPubMed
Pawlosky, RJ, Denkins, Y, Ward, G & Salem, N (1997) Retinal and brain accretion of long-chain polyunsaturated fatty acids in developing felines: the effect of corn oil-based maternal diets. Am J Clin Nutr 65, 465472.CrossRefGoogle ScholarPubMed
Sastry, P (1985) Lipid of nervous tissue:composition and metabolism. Prog Lipid Res 24, 69176.CrossRefGoogle Scholar
Uauy, RD, Birch, DG, Birch, EE, Tyson, JE & Hoffman, DR (1990) Effect of dietary omega-3 fatty acids on retinal function of very low birth weight neonates. Pediatr Res 28, 485492.CrossRefGoogle ScholarPubMed
Wainwright, PE, Huang, YS, Coscina, DV & Levesque, SMcCutcheon, D (1994) Brain and behavioral effect of dietary n -3 deficiency in mice: a three generation study. Dev Psychobiol 27, 467487.CrossRefGoogle Scholar
Wainwright, PE, Xing, HC, Mutsaers, L, McCutcheon, D & 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. J Nutr 127, 184193.CrossRefGoogle Scholar
Wheeler, TG, Benolken, RM & Anderson, RE (1975) Visual membrane: specificity of fatty acid precursors for the electrical response to illumination. Science 188, 13121314.CrossRefGoogle ScholarPubMed
Willatts, P, Forsyth, JS, Dimodugno, MK, Varma, S & Colvin, M (1998) Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age. Lancet 352, 688691.CrossRefGoogle ScholarPubMed