Is docosahexaenoic acid, an n−3 long-chain polyunsaturated fatty acid, required for development of normal brain function? An overview of evidence from cognitive and behavioral tests in humans and animals

Kolb, 2001, An introduction to brain and behavior

Beard, 2003, Iron status and neural functioning, Annu Rev Nutr, 23, 41, 10.1146/annurev.nutr.23.020102.075739

Black, 2003, The evidence linking zinc deficiency with children’s cognitive and motor functioning, J Nutr, 133, 1473S, 10.1093/jn/133.5.1473S

Lauritzen, 2001, The essentiality of long-chain n−3 fatty acids in relation to development and function of the brain and retina, Prog Lipid Res, 40, 1, 10.1016/S0163-7827(00)00017-5

Mattson, 2003, Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders, Trends Neurosci, 26, 137, 10.1016/S0166-2236(03)00032-8

Morris, 2003, Homocysteine and Alzheimer’s disease, Lancet Neurol, 2, 425, 10.1016/S1474-4422(03)00438-1

Zeisel, 2000, Choline: needed for normal development of memory, J Am Coll Nutr, 19, 528S, 10.1080/07315724.2000.10718976

Meck, 2003, Metabolic imprinting of choline by its availability during gestation: implications for memory and attentional processing across the lifespan, Neurosci Biobehav Rev, 27, 385, 10.1016/S0149-7634(03)00069-1

Giacobini, 2003, Cholinergic function and Alzheimer’s disease, Int J Geriatr Psychiatry, 18, S1, 10.1002/gps.935

Benton, 2001, Micro-nutrient supplementation and the intelligence of children, Neurosci Biobehav Rev, 25, 297, 10.1016/S0149-7634(01)00015-X

Schoenthaler, 2000, The effect of vitamin-mineral supplementation on the intelligence of American schoolchildren: a randomized, double-blind placebo-controlled trial, J Altern Complement Med, 6, 19, 10.1089/acm.2000.6.19

Bodnar, 2002, Low income postpartum women are at risk of iron deficiency, J Nutr, 132, 2298, 10.1093/jn/132.8.2298

Bogen, 2001, Outcome of children identified as anemic by routine screening in an inner-city clinic, Arch Pediatr Adolesc Med, 155, 366, 10.1001/archpedi.155.3.366

Siega-Riz, 2001, Dietary trends among low socioeconomic status women of childbearing age in the United States from 1977 to 1996: a comparison among ethnic groups, J Am Med Womens Assoc, 56, 44

Lee, 2001, Nutritional and health consequences are associated with food insecurity among U.S. elderly persons, J Nutr, 131, 1503, 10.1093/jn/131.5.1503

Dixon, 2001, Dietary intakes and serum nutrients differ between adults from food-insufficient and food-sufficient families: third National Health and Nutrition Examination Survey, 1988–1994, J Nutr, 131, 1232, 10.1093/jn/131.4.1232

Kumanyika, 2001, Preventive nutrition issues in ethnic and socioeconomic groups in the United States, Primary and secondary preventive nutrition, 325, 10.1007/978-1-59259-039-1_19

Eden, 1997, Mir MA. Iron deficiency in 1- to 3-year-old children. A pediatric failure?, Arch Pediatr Adolesc Med, 151, 986, 10.1001/archpedi.1997.02170470020003

Liu, 1996, African American and white differences in nutritional status among low-income women attending public health clinics, J Health Care Poor Underserved, 7, 323, 10.1353/hpu.2010.0392

Ames, 2004, A role for supplements in optimizing health: the metabolic tune-up, Arch Biochem Biophys, 423, 227, 10.1016/j.abb.2003.11.002

Ames, 2003, The metabolic tune-up: metabolic harmony and disease prevention, J Nutr, 133, 15445

Svennerholm, 1968, Distribution and fatty acid composition of phosphoglycerides in normal human brain, J Lipid Res, 9, 570, 10.1016/S0022-2275(20)42702-6

Anderson, 1975, Lipids of ocular tissues—X. Lipid composition of subcellular fractions of bovine retina, Vision Res, 15, 1087, 10.1016/0042-6989(75)90005-X

Martin, 1992, Changing fatty acid content of growth cone lipids prior to synaptogenesis, J Neurochem, 59, 318, 10.1111/j.1471-4159.1992.tb08906.x

Sastry, 1985, Lipids of nervous tissue: composition and metabolism, Prog Lipid Res, 24, 69, 10.1016/0163-7827(85)90011-6

Giusto, 2000, Lipid metabolism in vertebrate retinal rod outer segments, Prog Lipid Res, 39, 315, 10.1016/S0163-7827(00)00009-6

Martinez, 1992, Tissue levels of polyunsaturated fatty acids during early human development, J Pediatr, 120, S129, 10.1016/S0022-3476(05)81247-8

Clandinin, 1980, Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements, Early Hum Dev, 4, 121, 10.1016/0378-3782(80)90015-8

Bhattacharya, 1989, Prostaglandins modulate central serotonergic neurotransmission, Indian J Exp Biol, 27, 393

2002, Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids (macronutrients)

Wainwright, 1997, Essential fatty acids and behaviour: is there a role for eicosanoids?, Handbook of essential fatty acid biology: biochemistry, physiology and behavioural neurobiology, 299, 10.1007/978-1-4757-2582-7_14

Delion, 1996, Durand G. alpha-Linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex, J Neurochem, 66, 1582, 10.1046/j.1471-4159.1996.66041582.x

Aid, 2003, Effect of a diet-induced n−3 PUFA depletion on cholinergic parameters in the rat hippocampus, J Lipid Res, 44, 1545, 10.1194/jlr.M300079-JLR200

Kodas, 2004, Serotoninergic neurotransmission is affected by n−3 polyunsaturated fatty acids in the rat, J Neurochem, 89, 695, 10.1111/j.1471-4159.2004.02401.x

Zimmer, 2000, Modification of dopamine neurotransmission in the nucleus accumbens of rats deficient in n−3 polyunsaturated fatty acids, J Lipid Res, 41, 32, 10.1016/S0022-2275(20)32071-X

Zimmer, 2002, The dopamine mesocorticolimbic pathway is affected by deficiency in n−3 polyunsaturated fatty acids, Am J Clin Nutr, 75, 662, 10.1093/ajcn/75.4.662

de la Presa Owens, 1999, Docosahexaenoic and arachidonic acid prevent a decrease in dopaminergic and serotoninergic neurotransmitters in frontal cortex caused by a linoleic and alpha-linolenic acid deficient diet in formula-fed piglets, J Nutr, 129, 2088, 10.1093/jn/129.11.2088

Ng, 2003, Behavioral responses are altered in piglets with decreased frontal cortex docosahexaenoic acid, J Nutr, 133, 3222, 10.1093/jn/133.10.3222

Lesa, 2003, Long chain polyunsaturated fatty acids are required for efficient neurotransmission in C. elegans, J Cell Sci, 116, 4965, 10.1242/jcs.00918

Levant, 2004, Decreased brain docosahexaenoic acid during development alters dopamine-related behaviors in adult rats that are differentially affected by dietary remediation, Behav Brain Res, 152, 49

Ikemoto, 2000, Dietary n−3 fatty acid deficiency decreases nerve growth factor content in rat hippocampus, Neurosci Lett, 285, 99, 10.1016/S0304-3940(00)01035-1

Barcelo-Coblijn, 2003, Gene expression and molecular composition of phospholipids in rat brain in relation to dietary n−6 to n−3 fatty acid ratio, Biochim Biophys Acta, 1632, 72, 10.1016/S1388-1981(03)00064-7

Mitchell, 2003, DHA-rich phospholipids optimize G-protein-coupled signaling, J Pediatr, 143, S80, 10.1067/S0022-3476(03)00405-0

Bowen, 2002, Dietary low linolenic acid compared with docosahexaenoic acid alter synaptic plasma membrane phospholipid fatty acid composition and sodium-potassium ATPase kinetics in developing rats, J Neurochem, 83, 764, 10.1046/j.1471-4159.2002.01156.x

Ahmad, 2002, A decrease in cell size accompanies a loss of docosahexaenoate in the rat hippocampus, Nutr Neurosci, 5, 103, 10.1080/10284150290018973

Ahmad, 2002, Decrease in neuron size in docosahexaenoic acid-deficient brain, Pediatr Neurol, 26, 210, 10.1016/S0887-8994(01)00383-6

Kitajka, 2004, Effects of dietary omega-3 polyunsaturated fatty acids on brain gene expression, Proc Natl Acad Sci U S A, 101, 10931, 10.1073/pnas.0402342101

Innis, 2000, The role of dietary n−6 and n−3 fatty acids in the developing brain, Dev Neurosci, 22, 474, 10.1159/000017478

Salem, 2001, Mechanisms of action of docosahexaenoic acid in the nervous system, Lipids, 36, 945, 10.1007/s11745-001-0805-6

Salvati, 2000, lipids and brain development, Dev Neurosci, 22, 481, 10.1159/000017479

Sinclair, 2002, What is the role of alpha-linolenic acid for mammals?, Lipids, 37, 1113, 10.1007/s11745-002-1008-x

Innis, 2003, Perinatal biochemistry and physiology of long-chain polyunsaturated fatty acids, J Pediatr, 143, S1, 10.1067/S0022-3476(03)00396-2

Kurlak, 1999, Plausible explanations for effects of long-chain polyunsaturated fatty acids (LCPUFA) on neonates, Arch Dis Child Fetal Neonatal Ed, 80, F148, 10.1136/fn.80.2.F148

Gibson, 2001, Long-chain polyunsaturated fatty acids in breast milk: are they essential?, Adv Exp Med Biol, 501, 375, 10.1007/978-1-4615-1371-1_46

Das, 2003, Long-chain polyunsaturated fatty acids in the growth and development of the brain and memory, Nutrition, 19, 62, 10.1016/S0899-9007(02)00852-3

Chalon, 2001, Polyunsaturated fatty acids and cerebral function: focus on monoaminergic neurotransmission, Lipids, 36, 937, 10.1007/s11745-001-0804-7

Carlson, 1999, Polyunsaturated fatty acid status and neurodevelopment: a summary and critical analysis of the literature, Lipids, 34, 171, 10.1007/s11745-999-0351-2

Tanabe, 2004, Improvement of spatial cognition with dietary docosahexaenoic acid is associated with an increase in Fos expression in rat CA1 hippocampus, Clin Exp Pharmacol Physiol, 31, 700, 10.1111/j.1440-1681.2004.04068.x

Calderon, 2004, Docosahexaenoic acid promotes neurite growth in hippocampal neurons, J Neurochem, 90, 979, 10.1111/j.1471-4159.2004.02520.x

Anderson, 1974, Polyunsaturated fatty acids of photoreceptor membranes, Exp Eye Res, 18, 205, 10.1016/0014-4835(74)90149-3

Benolken, 1973, Membrane fatty acids associated with the electrical response in visual excitation, Science, 182, 1253, 10.1126/science.182.4118.1253

Bourre, 1989, The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats, J Nutr, 119, 1880, 10.1093/jn/119.12.1880

Neuringer, 1984, Dietary omega-3 fatty acid deficiency and visual loss in infant rhesus monkeys, J Clin Invest, 73, 272, 10.1172/JCI111202

Neuringer, 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 U S A, 83, 4021, 10.1073/pnas.83.11.4021

Wheeler, 1975, Visual membranes: specificity of fatty acid precursors for the electrical response to illumination, Science, 188, 1312, 10.1126/science.1145197

Birch, 1992, Retinal development in very-low-birth-weight infants fed diets differing in omega-3 fatty acids, Invest Ophthalmol Vis Sci, 33, 2365

Birch, 1992, Dietary essential fatty acid supply and visual acuity development, Invest Ophthalmol Vis Sci, 33, 3242

Carlson, 1993, Visual-acuity development in healthy preterm infants: effect of marine-oil supplementation, Am J Clin Nutr, 58, 35, 10.1093/ajcn/58.1.35

Uauy, 2003, Term infant studies of DHA and ARA supplementation on neurodevelopment: results of randomized controlled trials, J Pediatr, 143, S17, 10.1067/S0022-3476(03)00398-6

SanGiovanni, 2000, Meta-analysis of dietary essential fatty acids and long-chain polyunsaturated fatty acids as they relate to visual resolution acuity in healthy preterm infants, Pediatrics, 105, 1292, 10.1542/peds.105.6.1292

San Giovanni, 2000, Dietary essential fatty acids, long-chain polyunsaturated fatty acids, and visual resolution acuity in healthy fullterm infants: a systematic review, Early Hum Dev, 57, 165, 10.1016/S0378-3782(00)00050-5

Uauy, 2001, Essential fatty acids in visual and brain development, Lipids, 36, 885, 10.1007/s11745-001-0798-1

Simmer, Longchain polyunsaturated fatty acid supplementation in preterm infants, Cochrane Database Syst Rev, 2004, CD000375

Simmer, 2004, Longchain polyunsaturated fatty acid supplementation in infants born at term, 1

Neuringer, 2003, Visual development: neural basis and new assessment methods, J Pediatr, 143, S87, 10.1067/S0022-3476(03)00406-2

Neuringer, 2000, Infant vision and retinal function in studies of dietary long-chain polyunsaturated fatty acids: methods, results, and implications, Am J Clin Nutr, 71, 256S, 10.1093/ajcn/71.1.256S

Gibson, 1999, Polyunsaturated fatty acids and infant visual development: a critical appraisal of randomized clinical trials, Lipids, 34, 179, 10.1007/s11745-999-0352-1

Gibson, 2001, Randomized trials with polyunsaturated fatty acid interventions in preterm and term infants: functional and clinical outcomes, Lipids, 36, 873, 10.1007/s11745-001-0797-2

Koletzko, 2001, Long chain polyunsaturated fatty acids (LC-PUFA) and perinatal development, Acta Paediatr, 90, 460, 10.1111/j.1651-2227.2001.tb00452.x

Cockburn, 2003, Role of infant dietary long-chain polyunsaturated fatty acids, liposoluble vitamins, cholesterol and lecithin on psychomotor development, Acta Paediatr Suppl, 92, 19, 10.1111/j.1651-2227.2003.tb00660.x

Visioli, 2003, Dietary intake of fish vs. formulations leads to higher plasma concentrations of n−3 fatty acids, Lipids, 38, 415, 10.1007/s11745-003-1077-x

Kris-Etherton, 2000, Polyunsaturated fatty acids in the food chain in the United States, Am J Clin Nutr, 71, 179S, 10.1093/ajcn/71.1.179S

Zimmerman, 2001, Burgerstein’s handbook of nutrition: micronutrients in the prevention and therapy of disease

Simopoulos, 1999, Essential fatty acids in health and chronic disease, Am J Clin Nutr, 70, 560S, 10.1093/ajcn/70.3.560s

Carnielli, 1996, The very low birth weight premature infant is capable of synthesizing arachidonic and docosahexaenoic acids from linoleic and linolenic acids, Pediatr Res, 40, 169, 10.1203/00006450-199607000-00029

Salem, 1996, Arachidonic and docosahexaenoic acids are biosynthesized from their 18-carbon precursors in human infants, Proc Natl Acad Sci U S A, 93, 49, 10.1073/pnas.93.1.49

Sauerwald, 1997, New insights into the metabolism of long chain polyunsaturated fatty acids during infancy, Eur J Med Res, 2, 88

Uauy, 2000, Long chain polyunsaturated fatty acid formation in neonates: effect of gestational age and intrauterine growth, Pediatr Res, 47, 127, 10.1203/00006450-200001000-00022

Dutta-Roy, 2000, Transport mechanisms for long-chain polyunsaturated fatty acids in the human placenta, Am J Clin Nutr, 71, 315S, 10.1093/ajcn/71.1.315s

Putnam, 1982, The effect of variations in dietary fatty acids on the fatty acid composition of erythrocyte phosphatidylcholine and phosphatidylethanolamine in human infants, Am J Clin Nutr, 36, 106, 10.1093/ajcn/36.1.106

Uauy, 1999, Breast is best: human milk is the optimal food for brain development, Am J Clin Nutr, 70, 433, 10.1093/ajcn/70.4.433

Haggarty, 2004, Effect of placental function on fatty acid requirements during pregnancy, Eur J Clin Nutr, 58, 1559, 10.1038/sj.ejcn.1602016

Crawford, 2000, Placental delivery of arachidonic and docosahexaenoic acids: implications for the lipid nutrition of preterm infants, Am J Clin Nutr, 71, 275S, 10.1093/ajcn/71.1.275S

Innis, 2004, Polyunsaturated fatty acids in human milk: an essential role in infant development, Adv Exp Med Biol, 554, 27, 10.1007/978-1-4757-4242-8_5

Muskiet, 2004, Is docosahexaenoic acid (DHA) essential? Lessons from DHA status regulation, our ancient diet, epidemiology and randomized controlled trials, J Nutr, 134, 183, 10.1093/jn/134.1.183

Carlson, 2001, Docosahexaenoic acid and arachidonic acid in infant development, Semin Neonatol, 6, 437, 10.1053/siny.2001.0093

Cunnane, 2003, Problems with essential fatty acids: time for a new paradigm?, Prog Lipid Res, 42, 544, 10.1016/S0163-7827(03)00038-9

Hornstra, 2000, Essential fatty acids in mothers and their neonates, Am J Clin Nutr, 71, 1262S, 10.1093/ajcn/71.5.1262s

Simopoulos, 1999, Workshop on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids, J Am Coll Nutr, 18, 487, 10.1080/07315724.1999.10718888

Koletzko, 1999, Long-chain polyunsaturated fatty acids in diets for infants: choices for recommending and regulating bodies and for manufacturers of dietary products, Lipids, 34, 215, 10.1007/s11745-999-0356-x

Greiner, 2003, Docosapentaenoic acid does not completely replace DHA in n−3 FA-deficient rats during early development, Lipids, 38, 431, 10.1007/s11745-003-1080-2

Wainwright, 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, 184, 10.1093/jn/127.1.184

Wainwright, 1994, The effects of dietary fatty acid composition combined with environmental enrichment on brain and behavior in mice, Behav Brain Res, 60, 125, 10.1016/0166-4328(94)90139-2

Wainwright, 1994, Brain and behavioral effects of dietary n−3 deficiency in mice: a three generational study, Dev Psychobiol, 27, 467, 10.1002/dev.420270705

Wainwright, 1999, Water maze performance is unaffected in artificially reared rats fed diets supplemented with arachidonic acid and docosahexaenoic acid, J Nutr, 129, 1079, 10.1093/jn/129.5.1079

Byard, 1995, Sudden infant death syndrome: effect of breast and formula feeding on frontal cortex and brainstem lipid composition, J Paediatr Child Health, 31, 14, 10.1111/j.1440-1754.1995.tb02904.x

Makrides, 1994, Fatty acid composition of brain, retina, and erythrocytes in breast- and formula-fed infants, Am J Clin Nutr, 60, 189, 10.1093/ajcn/60.2.189

Jamieson, 1999, Infant cerebellar gray and white matter fatty acids in relation to age and diet, Lipids, 34, 1065, 10.1007/s11745-999-0458-5

Farquharson, 1992, Infant cerebral cortex phospholipid fatty-acid composition and diet, Lancet, 340, 810, 10.1016/0140-6736(92)92684-8

Farquharson, 1995, Effect of diet on the fatty acid composition of the major phospholipids of infant cerebral cortex, Arch Dis Child, 72, 198, 10.1136/adc.72.3.198

Cunnane, 2000, Breast-fed infants achieve a higher rate of brain and whole body docosahexaenoate accumulation than formula-fed infants not consuming dietary docosahexaenoate, Lipids, 35, 105, 10.1007/s11745-000-0501-6

Sarkadi-Nagy, 2003, The influence of prematurity and long chain polyunsaturate supplementation in 4-week adjusted age baboon neonate brain and related tissues, Pediatr Res, 54, 244, 10.1203/01.PDR.0000072795.38990.F2

Carlson, 1996, Visual acuity and fatty acid status of term infants fed human milk and formulas with and without docosahexaenoate and arachidonate from egg yolk lecithin, Pediatr Res, 39, 882, 10.1203/00006450-199605000-00024

Boehm, 1996, Docosahexaenoic and arachidonic acid content of serum and red blood cell membrane phospholipids of preterm infants fed breast milk, standard formula or formula supplemented with n−3 and n−6 long-chain polyunsaturated fatty acids, Eur J Pediatr, 155, 410, 10.1007/BF01955275

Schneider, 1992, Neurobehavioral assessment in rhesus monkey neonates (Macaca mulatta): developmental changes, behavioral stability, and early experience, Infant Behav Dev, 15, 155, 10.1016/0163-6383(92)80021-L

Prechtl, 2001, General movement assessment as a method of developmental neurology: new paradigms and their consequences. The 1999 Ronnie MacKeith Lecture, Dev Med Child Neurol, 43, 836, 10.1017/S0012162201001529

Freudigman, 1993, Infant sleep during the first postnatal day: an opportunity for assessment of vulnerability, Pediatrics, 92, 373

Carlson, 2000, Behavioral methods used in the study of long-chain polyunsaturated fatty acid nutrition in primate infants, Am J Clin Nutr, 71, 268S, 10.1093/ajcn/71.1.268s

Wainwright, 2002, Dietary essential fatty acids and brain function: a developmental perspective on mechanisms, Proc Nutr Soc, 61, 61, 10.1079/PNS2001130

Gibson, 1999, Long-chain polyunsaturated fatty acids and infant development, Lancet, 354, 1919, 10.1016/S0140-6736(99)00300-1

Carlson, 1996, Assessment of infant visual and cognitive function in relation to long chain polyunsaturated fatty acids

Gibson, 2000, n−3 Polyunsaturated fatty acid requirements of term infants, Am J Clin Nutr, 71, 251S, 10.1093/ajcn/71.1.251s

Colombo, 1997, Individual differences in infant cognition: methods, measures and models, Developing brain and behavior: the role of lipids in infant formulas, 372, 10.1016/B978-012218870-1/50010-5

Willatts, 2000, The role of long-chain polyunsaturated fatty acids in infant cognitive development, Prostaglandins Leukot Essent Fatty Acids, 63, 95, 10.1054/plef.2000.0198

Forsyth, 1998, Do long-chain polyunsaturated fatty acids influence infant cognitive behaviour?, Biochem Soc Trans, 26, 252, 10.1042/bst0260252

Jacobson, 1999, Assessment of long-chain polyunsaturated fatty acid nutritional supplementation on infant neurobehavioral development and visual acuity, Lipids, 34, 151, 10.1007/s11745-999-0349-9

Burgard, 2003, Critical evaluation of the methodology employed in cognitive development trials, Acta Paediatr Suppl, 92, 6, 10.1111/j.1651-2227.2003.tb00658.x

Bayley, 1993, The Bayley Scales of Infant Development, revision, 1993

Allard, 1988, The Kaufman Assessment Battery for Children: a validity study with at-risk preschoolers, J Psychoeduc Assess, 6, 215, 10.1177/073428298800600304

Fenson, 1994, Variability in early communicative development, Monogr Soc Res Child Dev, 59, 1, 10.2307/1166093

Fagan, 1986, The Fagan Test of Infant Intelligence

Willatts, 1984, Stages in the development of intentional search by young infants, Dev Psychol, 20, 389, 10.1037/0012-1649.20.3.389

Willatts, 1997, Beyond the ‘couch potato’ infant: how infants use their knowledge to regulate action, solve problems, and achieve goals, Infant development: recent advances: Hove, 109

Reisbick, 1990, Polydipsia in rhesus monkeys deficient in omega-3 fatty acids, Physiol Behav, 47, 315, 10.1016/0031-9384(90)90149-X

Reisbick, 1994, Home cage behavior of rhesus monkeys with long-term deficiency of omega-3 fatty acids, Physiol Behav, 55, 231, 10.1016/0031-9384(94)90128-7

Reisbick, 1997, Visual attention in infant monkeys: effects of dietary fatty acids and age, Dev Psychol, 33, 387, 10.1037/0012-1649.33.3.387

Olton, 1977, Spatial memory and radial arm maze performance in rats, Learn Motiv, 8, 289, 10.1016/0023-9690(77)90054-6

Foreman, 1998, The radial arm maze: twenty years on, A handbook of spatial research paradigms and methodologies: Hove, 87

Hodges, 1996, Maze procedures: the radial-arm and water maze compared, Brain Res Cogn Brain Res, 3, 167, 10.1016/0926-6410(96)00004-3

Schenk, 1998, The Morris water maze (is not a maze), A handbook of spatial research paradigms and methodologies: Hove, 145

Morris, 1981, Spatial localization does not require the presence of local cues, Learn Motiv, 12, 239, 10.1016/0023-9690(81)90020-5

Lister, 1987, The use of a plus-maze to measure anxiety in the mouse, Psychopharmacology (Berl), 92, 180, 10.1007/BF00177912

Pellow, 1985, Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat, J Neurosci Methods, 14, 149, 10.1016/0165-0270(85)90031-7

Metz, 2005, Neuropsychological tests, The behavior of the laboratory rat: a handbook with tests, 475

Yamamoto, 1987, Effect of dietary alpha-linolenate/linoleate balance on brain lipid compositions and learning ability of rats, J Lipid Res, 28, 144, 10.1016/S0022-2275(20)38713-7

Wainwright, 1992, Do essential fatty acids play a role in brain and behavioral development?, Neurosci Biobehav Rev, 16, 193, 10.1016/S0149-7634(05)80180-0

Innis, 2000, Essential fatty acids in infant nutrition: lessons and limitations from animal studies in relation to studies on infant fatty acid requirements, Am J Clin Nutr, 71, 238S, 10.1093/ajcn/71.1.238S

Wainwright, 1998, Effects of dietary n−3 deficiency on amphetamine-conditioned place preference and working memory in the Morris water-maze, Nutr Neurosci, 1, 281, 10.1080/1028415X.1998.11747238

Jacobson, 2002, Breastfeeding and IQ: evaluation of the socio-environmental confounders, Acta Paediatr, 91, 258, 10.1111/j.1651-2227.2002.tb01708.x

Rey, 2003, Breastfeeding and cognitive development, Acta Paediatr Suppl, 92, 11, 10.1111/j.1651-2227.2003.tb00659.x

Innis, 1999, Maternal diet, length of gestation, and long-chain polyunsaturated fatty acid status of infants at birth, Am J Clin Nutr, 70, 181, 10.1093/ajcn.70.2.181

Reynolds, 2001, The evidence for breastfeeding: breastfeeding and brain development, Pediatr Clin North Am, 48, 159, 10.1016/S0031-3955(05)70291-1

Jain, 2002, How good is the evidence linking breastfeeding and intelligence?, Pediatrics, 109, 1044, 10.1542/peds.109.6.1044

Carlson, 1999, Long-chain polyunsaturated fatty acids and development of human infants, Acta Paediatr Suppl, 88, 72, 10.1111/j.1651-2227.1999.tb01304.x

Gibson, 2001, More research is needed to determine the effects of human milk on neonatal outcome, Pediatrics, 108, 465, 10.1542/peds.108.2.465

Anderson, 1999, Breast-feeding and cognitive development: a meta-analysis, Am J Clin Nutr, 70, 525, 10.1093/ajcn/70.4.525

Drane, 2000, A critical evaluation of the evidence on the association between type of infant feeding and cognitive development, Paediatr Perinat Epidemiol, 14, 349, 10.1046/j.1365-3016.2000.00301.x

Gordon, 2000, Breast-feeding, breast-milk feeding, and intelligence quotient, Am J Clin Nutr, 72, 1063, 10.1093/ajcn/72.4.1063a

Gomez-Sanchiz, 2003, Influence of breast-feeding on mental and psychomotor development, Clin Pediatr (Phila), 42, 35, 10.1177/000992280304200106

Jacobson, 1999, Breastfeeding effects on intelligence quotient in 4- and 11-year-old children, Pediatrics, e71, 103

Morley, 2004, Neurodevelopment in children born small for gestational age: a randomized trial of nutrient-enriched versus standard formula and comparison with a reference breastfed group, Pediatrics, 113, 515, 10.1542/peds.113.3.515

Auestad, 2001, Growth and development in term infants fed long-chain polyunsaturated fatty acids: a double-masked, randomized, parallel, prospective, multivariate study, Pediatrics, 108, 372, 10.1542/peds.108.2.372

Auestad, 2003, Visual, cognitive, and language assessments at 39 months: a follow-up study of children fed formulas containing long-chain polyunsaturated fatty acids to 1 year of age, Pediatrics, 112, e177, 10.1542/peds.112.3.e177

Bouwstra, 2003, Long-chain polyunsaturated fatty acids have a positive effect on the quality of general movements of healthy term infants, Am J Clin Nutr, 78, 313, 10.1093/ajcn/78.2.313

Lucas, 1999, Efficacy and safety of long-chain polyunsaturated fatty acid supplementation of infant-formula milk: a randomised trial, Lancet, 354, 1948, 10.1016/S0140-6736(99)02314-4

Makrides, 2000, A critical appraisal of the role of dietary long-chain polyunsaturated fatty acids on neural indices of term infants: a randomized, controlled trial, Pediatrics, 105, 32, 10.1542/peds.105.1.32

Fewtrell, 2002, Double-blind, randomized trial of long-chain polyunsaturated fatty acid supplementation in formula fed to preterm infants, Pediatrics, 110, 73, 10.1542/peds.110.1.73

Agostoni, 2001, Breastfeeding duration, milk fat composition and developmental indices at 1 year of life among breastfed infants, Prostaglandins Leukot Essent Fatty Acids, 64, 105, 10.1054/plef.2001.0248

Angelsen, 2001, Breast feeding and cognitive development at age 1 and 5 years, Arch Dis Child, 85, 183, 10.1136/adc.85.3.183

Bouwstra, 2003, Exclusive breastfeeding of healthy term infants for at least 6 weeks improves neurological condition, J Nutr, 133, 4243, 10.1093/jn/133.12.4243

Mortensen, 2002, The association between duration of breastfeeding and adult intelligence, JAMA, 287, 2365, 10.1001/jama.287.18.2365

Oddy, 2003, Breast feeding and cognitive development in childhood: a prospective birth cohort study, Paediatr Perinat Epidemiol, 17, 81, 10.1046/j.1365-3016.2003.00464.x

Quinn, 2001, The effect of breastfeeding on child development at 5 years: a cohort study, J Paediatr Child Health, 37, 465, 10.1046/j.1440-1754.2001.00702.x

Ribas-Fito, 2003, Breastfeeding, exposure to organochlorine compounds, and neurodevelopment in infants, Pediatrics, 111, e580, 10.1542/peds.111.5.e580

Richards, 2002, Long-term effects of breast-feeding in a national birth cohort: educational attainment and midlife cognitive function, Public Health Nutr, 5, 631, 10.1079/PHN2002338

Horwood, 2001, Breast milk feeding and cognitive ability at 7–8 years, Arch Dis Child Fetal Neonatal Ed, 84, F23, 10.1136/fn.84.1.F23

Rao, 2002, Effect of breastfeeding on cognitive development of infants born small for gestational age, Acta Paediatr, 91, 267, 10.1111/j.1651-2227.2002.tb01713.x

Smith, 2003, Influence of breastfeeding on cognitive outcomes at age 6–8 years: follow-up of very low birth weight infants, Am J Epidemiol, 158, 1075, 10.1093/aje/kwg257

Bakker, 2003, Long-chain polyunsaturated fatty acids at birth and cognitive function at 7 y of age, Eur J Clin Nutr, 57, 89, 10.1038/sj.ejcn.1601506

Ghys, 2002, Red blood cell and plasma phospholipid arachidonic and docosahexaenoic acid levels at birth and cognitive development at 4 years of age, Early Hum Dev, 69, 83, 10.1016/S0378-3782(02)00067-1

Forsyth, 2001, Long-chain polyunsaturated fatty acids in infant nutrition: effects on infant development, Curr Opin Clin Nutr Metab Care, 4, 123, 10.1097/00075197-200103000-00007

Uauy, 2001, Lipids and neurodevelopment, Nutr Rev, 59, S34, 10.1111/j.1753-4887.2001.tb05500.x

Uauy, 2001, Essential fatty acids in somatic growth and brain development, World Rev Nutr Diet, 89, 134, 10.1159/000059785

Fewtrell, 2004, Randomized, double-blind trial of long-chain polyunsaturated fatty acid supplementation with fish oil and borage oil in preterm infants, J Pediatr, 144, 471, 10.1016/j.jpeds.2004.01.034

Colombo, 2004, Maternal DHA and the development of attention in infancy and toddlerhood, Child Dev, 75, 1254, 10.1111/j.1467-8624.2004.00737.x

Cheruku, 2002, Higher maternal plasma docosahexaenoic acid during pregnancy is associated with more mature neonatal sleep-state patterning, Am J Clin Nutr, 76, 608, 10.1093/ajcn/76.3.608

Voigt, 2002, Relationship between omega-3 long-chain polyunsaturated fatty acid status during early infancy and neurodevelopmental status at 1 year of age, J Hum Nutr Diet, 15, 111, 10.1046/j.1365-277X.2002.00341.x

Innis, 2001, Are human milk long-chain polyunsaturated fatty acids related to visual and neural development in breast-fed term infants?, J Pediatr, 139, 532, 10.1067/mpd.2001.118429

Birch, 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, 174, 10.1017/S0012162200000311

Birch, 2002, A randomized controlled trial of long-chain polyunsaturated fatty acid supplementation of formula in term infants after weaning at 6 wk of age, Am J Clin Nutr, 75, 570, 10.1093/ajcn/75.3.570

Helland, 2001, Similar effects on infants of n−3 and n−6 fatty acids supplementation to pregnant and lactating women, Pediatrics, 108, E82, 10.1542/peds.108.5.e82

Helland, 2003, Maternal supplementation with very-long-chain n−3 fatty acids during pregnancy and lactation augments children’s IQ at 4 years of age, Pediatrics, 111, e39, 10.1542/peds.111.1.e39

Hoffman, 2003, Visual function in breast-fed term infants weaned to formula with or without long-chain polyunsaturates at 4 to 6 months: a randomized clinical trial, J Pediatr, 142, 669, 10.1067/mpd.2003.213

Heird, 2001, The role of polyunsaturated fatty acids in term and preterm infants and breastfeeding mothers, Pediatr Clin North Am, 48, 173, 10.1016/S0031-3955(05)70292-3

Makrides, 2000, A randomized trial of different ratios of linoleic to alpha-linolenic acid in the diet of term infants: effects on visual function and growth, Am J Clin Nutr, 71, 120, 10.1093/ajcn/71.1.120

O’Connor, 2001, Growth and development in preterm infants fed long-chain polyunsaturated fatty acids: a prospective, randomized controlled trial, Pediatrics, 108, 359, 10.1542/peds.108.2.359

Williams, 2001, Stereoacuity at age 3.5 y in children born full-term is associated with prenatal and postnatal dietary factors: a report from a population-based cohort study, Am J Clin Nutr, 73, 316, 10.1093/ajcn/73.2.316

Scott, 1998, Formula supplementation with long-chain polyunsaturated fatty acids: are there developmental benefits?, Pediatrics, 102, E59, 10.1542/peds.102.5.e59

Auestad, 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, 1, 10.1203/00006450-199701000-00001

Birch, 1998, Visual acuity and the essentiality of docosahexaenoic acid and arachidonic acid in the diet of term infants, Pediatr Res, 44, 201, 10.1203/00006450-199808000-00011

Makrides, 2001, Perinatal characteristics may influence the outcome of visual acuity, Lipids, 36, 897, 10.1007/s11745-001-0799-0

O’Connor, 2003, Growth and development of premature infants fed predominantly human milk, predominantly premature infant formula, or a combination of human milk and premature formula, J Pediatr Gastroenterol Nutr, 37, 437, 10.1097/00005176-200310000-00008

Raven, 2000, The Raven’s progressive matrices: change and stability over culture and time, Cognit Psychol, 41, 1, 10.1006/cogp.1999.0735

Raven, 1998, Manual for Raven’s progressive matrices and vocabulary scales, Section 1: general overview

Willatts, 1998, Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age, Lancet, 352, 688, 10.1016/S0140-6736(97)11374-5

Werkman, 1996, A randomized trial of visual attention of preterm infants fed docosahexaenoic acid until nine months, Lipids, 31, 91, 10.1007/BF02522417

Carlson, 1996, A randomized trial of visual attention of preterm infants fed docosahexaenoic acid until two months, Lipids, 31, 85, 10.1007/BF02522416

Willatts, 1998, Influence of long-chain polyunsaturated fatty acids on infant cognitive function, Lipids, 33, 973, 10.1007/s11745-998-0294-7

Wainwright, 2001, The role of nutritional factors in behavioural development in laboratory mice, Behav Brain Res, 125, 75, 10.1016/S0166-4328(01)00286-8

Wainwright, 2000, Nutrition and behaviour: the role of n−3 fatty acids in cognitive function, Br J Nutr, 83, 337

Reisbick, 1997, Omega-3 fatty acid deficiency and behavior: a critical review and future directions for research, Handbook of essential fatty acid biology: biochemistry, physiology and behavioral neurobiology, 397, 10.1007/978-1-4757-2582-7_17

Moriguchi, 2003, Recovery of brain docosahexaenoate leads to recovery of spatial task performance, J Neurochem, 87, 297, 10.1046/j.1471-4159.2003.01966.x

Catalan, 2002, Cognitive deficits in docosahexaenoic acid-deficient rats, Behav Neurosci, 116, 1022, 10.1037/0735-7044.116.6.1022

Greiner, 2001, Olfactory discrimination deficits in n−3 fatty acid-deficient rats, Physiol Behav, 72, 379, 10.1016/S0031-9384(00)00437-6

Moriguchi, 2000, Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration, J Neurochem, 75, 2563, 10.1046/j.1471-4159.2000.0752563.x

Greiner, 1999, Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks, Lipids, 34, S239, 10.1007/BF02562305

Carrie, 2002, Docosahexaenoic acid-rich phospholipid supplementation: effect on behavior, learning ability, and retinal function in control and n−3 polyunsaturated fatty acid deficient old mice, Nutr Neurosci, 5, 43, 10.1080/10284150290007074

Frances, 2000, Nutritional (n−3) polyunsaturated fatty acids influence the behavioral responses to positive events in mice, Neurosci Lett, 285, 223, 10.1016/S0304-3940(00)01065-X

Carrie, 2000, Diets containing long-chain n−3 polyunsaturated fatty acids affect behaviour differently during development than ageing in mice, Br J Nutr, 83, 439

Carrie, 2000, Phospholipid supplementation reverses behavioral and biochemical alterations induced by n−3 polyunsaturated fatty acid deficiency in mice, J Lipid Res, 41, 473, 10.1016/S0022-2275(20)34486-2

Frances, 1996, Effect of dietary alpha-linolenic acid deficiency on habituation, Life Sci, 58, 1805, 10.1016/0024-3205(96)00164-6

Frances, 1995, Effects of dietary alpha-linolenic acid deficiency on neuromuscular and cognitive functions in mice, Life Sci, 57, 1935, 10.1016/0024-3205(95)02180-Q

Frances, 1996, Influence of a dietary alpha-linolenic acid deficiency on learning in the Morris water maze and on the effects of morphine, Eur J Pharmacol, 298, 217, 10.1016/0014-2999(95)00825-X

Ikemoto, 2001, Reversibility of n−3 fatty acid deficiency-induced alterations of learning behavior in the rat: level of n−6 fatty acids as another critical factor, J Lipid Res, 42, 1655, 10.1016/S0022-2275(20)32220-3

Okaniwa, 1996, A high linoleate and a high alpha-linolenate diet induced changes in learning behavior of rats. Effects of a shift in diets and reversal of training stimuli, Biol Pharm Bull, 19, 536, 10.1248/bpb.19.536

Yoshida, 1997, Synaptic vesicle ultrastructural changes in the rat hippocampus induced by a combination of alpha-linolenate deficiency and a learning task, J Neurochem, 68, 1261, 10.1046/j.1471-4159.1997.68031261.x

Umezawa, 1999, High-linoleate and high-α-linolenate diets affect learning ability and natural behavior in SAMR1 mice, J Nutr, 129, 431, 10.1093/jn/129.2.431

Umezawa, 1995, Dietary alpha-linolenate/linoleate balance influences learning and memory in the senescence-accelerated mouse (SAM), Brain Res, 669, 225, 10.1016/0006-8993(94)01250-L

Gamoh, 2001, Chronic administration of docosahexaenoic acid improves the performance of radial arm maze task in aged rats, Clin Exp Pharmacol Physiol, 28, 266, 10.1046/j.1440-1681.2001.03437.x

Gamoh, 1999, Chronic administration of docosahexaenoic acid improves reference memory-related learning ability in young rats, Neuroscience, 93, 237, 10.1016/S0306-4522(99)00107-4

Wainwright, 2003, Effects of high-gamma-linolenic acid canola oil compared with borage oil on reproduction, growth, and brain and behavioral development in mice, Lipids, 38, 171, 10.1007/s11745-003-1048-2

Clements, 2003, Spontaneously hypertensive and Wistar Kyoto rats differ in delayed matching-to-place performance and response to dietary long-chain polyunsaturated fatty acids, Dev Psychobiol, 43, 57, 10.1002/dev.10121

Wainwright, 1999, An imbalance of dietary essential fatty acids retards behavioral development in mice, Physiol Behav, 66, 833, 10.1016/S0031-9384(99)00028-1

Takeuchi, 2003, Possible regulatory mechanism of DHA-induced anti-stress reaction in rats, Brain Res, 964, 136, 10.1016/S0006-8993(02)04113-6

Takeuchi, 2002, Influence of a dietary n−3 fatty acid deficiency on the cerebral catecholamine contents, EEG and learning ability in rat, Behav Brain Res, 131, 193, 10.1016/S0166-4328(01)00392-8

Nakashima, 1993, Effect of a high linoleate and a high alpha-linolenate diet on general behavior and drug sensitivity in mice, J Lipid Res, 34, 239, 10.1016/S0022-2275(20)40751-5

Yonekubo, 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, Biosci Biotechnol Biochem, 57, 253, 10.1271/bbb.57.253

Yonekubo, 1994, Effects of dietary fish oil during the fetal and postnatal periods on the learning ability of postnatal rats, Biosci Biotechnol Biochem, 58, 799, 10.1271/bbb.58.799

Champoux, 2002, Fatty acid formula supplementation and neuromotor development in rhesus monkey neonates, Pediatr Res, 51, 273, 10.1203/00006450-200203000-00003

Yamamoto, 1988, Effect of the dietary alpha-linolenate/linoleate balance on lipid compositions and learning ability of rats. II, Discrimination process, extinction process, and glycolipid compositions J Lipid Res, 29, 1013

Bourre, 2004, Roles of unsaturated fatty acids (especially omega-3 fatty acids) in the brain at various ages and during ageing, J Nutr Health Aging, 8, 163

Yehuda, 2003, Omega-6/omega-3 ratio and brain-related functions, Omega-6/omega-3 essential fatty acid ratio: the scientific evidence, 37, 10.1159/000073791

Wainwright, 1997, Early nutrition and behavior: a conceptual framework for critical analysis of research, Developing brain and behavior: the role of lipids in infant formula, 387, 10.1016/B978-012218870-1/50011-7

Wauben, 1999, The influence of neonatal nutrition on behavioral development: a critical appraisal, Nutr Rev, 57, 35, 10.1111/j.1753-4887.1999.tb01776.x

Brenna, 2002, Efficiency of conversion of alpha-linolenic acid to long chain n−3 fatty acids in man, Curr Opin Clin Nutr Metab Care, 5, 127, 10.1097/00075197-200203000-00002

Kwik-Uribe, 2000, Chronic marginal iron intakes during early development in mice result in persistent changes in dopamine metabolism and myelin composition, J Nutr, 130, 2821, 10.1093/jn/130.11.2821

Crawford, 2003, The potential role for arachidonic and docosahexaenoic acids in protection against some central nervous system injuries in preterm infants, Lipids, 38, 303, 10.1007/s11745-003-1065-1

Lopez-Garcia, 2004, Consumption of (n−3) fatty acids is related to plasma biomarkers of inflammation and endothelial activation in women, J Nutr, 134, 1806, 10.1093/jn/134.7.1806

Simopoulos, 2003, Omega-6/omega-3 essential fatty acid ratio: the scientific evidence, 10.1159/isbn.978-3-318-01018-3

Wainwright, 1998, Issues of design and analysis relating to the use of multiparous species in developmental nutritional studies, J Nutr, 128, 661, 10.1093/jn/128.3.661

Willis, 1981, Unanswered questions in EFA and PG research, Prog Lipid Res, 20, 839, 10.1016/0163-7827(81)90159-4

Murthy, 2002, Differential effects of n−3 fatty acid deficiency on phospholipid molecular species composition in the rat hippocampus, J Lipid Res, 43, 611, 10.1016/S0022-2275(20)31491-7

Frick, 2000, Mice are not little rats: species differences in a one-day water maze task, Neuroreport, 11, 3461, 10.1097/00001756-200011090-00013

Whishaw, 1996, Of mice and mazes: similarities between mice and rats on dry land but not water mazes, Physiol Behav, 60, 1191, 10.1016/S0031-9384(96)00176-X

Whishaw, 1995, A comparison of rats and mice in a swimming pool place task and matching to place task: some surprising differences, Physiol Behav, 58, 687, 10.1016/0031-9384(95)00110-5

Ward, 1998, Long-chain polyunsaturated fatty acid levels in formulae influence deposition of docosahexaenoic acid and arachidonic acid in brain and red blood cells of artificially reared neonatal rats, J Nutr, 128, 2473

Jorgensen, 1999, The role of long-chain polyunsaturated fatty acids in neonatal nutrition, Acta Paediatr, 88, 916, 10.1111/j.1651-2227.1999.tb00072.x

Hill, 1971, Principles of medical statistics, 9th edition