Omega-3 Fatty Acid Deficiency and Behavior

A Critical Review and Directions for Future Research
  • Sydney Reisbick
  • Martha Neuringer


Much of the impetus for studies of omega-3 fatty acid (FA) deficiency originates from the need to determine whether these FA should be added to human infant formulas, and if so in what form: as the precursor omega-3 FA, linolenic acid (18:3 omega-3, or as the derived form, docosahexaenoic acid ([DHA], 22:6 omega-3), which is present at high levels in retina and brain. After early studies showed effects of omega-3 FA deficiency on visual development in monkeys (Neuringer et al., 1984, 1986), levels of linolenic acid were increased in many infant formulas, especially those in the United States, beginning in 1987. However, DHA levels in erythrocytes of human infants fed formulas with either low or high levels of linolenic acid were lower than the DHA levels of infants who received DHA directly either in breast milk or in fish oil supplemented formulas (Pita et al., 1988; Carlson et al., 1986; Makrides et al., 1993; Uauy et al., 1994). This finding suggested that human infants do not elongate and desp.turate an adequate amount of linolenic acid into DHA. This hypothesis was supported by more recent postmortem studies that reported lower DHA levels in the cerebral cortex of infants fed formulas with linolenic acid than in breast-fed infants (Farquharson et al., 1992; Makrides et al., 1994).


Morris Water Maze Performance Factor Human Infant Horne Cage Novelty Preference 
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  1. Abbey, H. and Howard, E. (1973) Statistical procedures in developmental studies on species with multiple offspring. Dev. Psychobiol. 6, 329 - 335.PubMedCrossRefGoogle Scholar
  2. Almeida, S., Garcia, R., and Oliveira, L. (1993) Effects of early protein malnutrition and repeated testing upon locomotor and exploratory behaviors in the elevated plus-maze. Physiol. Behay. 54, 749 - 752.CrossRefGoogle Scholar
  3. Ammouche, A., Youyou, Y., Durand, G., and Bourre, J. M. (1994) Effect of dietary fats on nucleoside triphosphatase activity and nuclear membrane fatty acid composition of rats during development. Ann. Nutr. Metab. 38, 132 - 140.PubMedCrossRefGoogle Scholar
  4. Amt, J., Bogeso, K. P., Hyttel, J., and Meier, E. (1988) Relative dopamine D1 and D2 receptor affinity and efficacy determine whether dopamine agonists induce hyperactivity or oral stereotypy. Pharmacol. Toxicol. 62, 121 - 130.CrossRefGoogle Scholar
  5. Banks, K. E. and Gratton, A. (1995) Possible involvement of medial prefrontal cortex in amphetamine-induced sensitization of mesolimbic dopamine function. Eur. J. Pharmacol. 282, 157 - 167.PubMedCrossRefGoogle Scholar
  6. Bedi, K. S. (1992) Spatial learning ability of rats undernourished during early postnatal life. Physiol. Behay. 51, 1001 - 1007.CrossRefGoogle Scholar
  7. Benjamin, J., Li, L., Patterson, C., Greenberg, B. D., Murphy, D. L., and Hamer, D. H. (1996) Population and familial association between the D4 dopamine receptor gene and measures of novelty seeking. Nature Genetics 12, 81 - 84.PubMedCrossRefGoogle Scholar
  8. Birch, D. G., Birch, E. E., Hoffman, D. R., and Uauy, R. D. (1992a) Retinal development in very-low-birth-weight infants fed diets differing in omega-3 fatty acids. Invest. Ophthalmol. Vis. Sci. 33, 2365 - 2376.PubMedGoogle Scholar
  9. Birch, E., Birch, D., Hoffman, D., Hale, L., Everett, M., and Uauy, R. (1993) Breast-feeding and optimal visual development. J. Pediatr. Ophthalmol. Strabismus 30, 33 - 38.PubMedGoogle Scholar
  10. Birch, E. E., Birch, D. G., Hoffman, D. R., and Uauy, R. D. (1992b) Dietary essential fatty acid supply and visual acuity development. Invest. Ophthalmol. Vis. Sci. 33, 3242 - 3253.PubMedGoogle Scholar
  11. Blum, K., Cull, J. G., Braverman, E. R., and Comings, D. E. (1996) Reward deficiency syndrome. Am. Sci. 84, 132 - 145.Google Scholar
  12. Bourre, J.-M., Dumont, O. S., Piciotti, M. J., Pascal, G. A., and Durand, G. A. (1992) Dietary a-linolenic acid deficiency in adult rats for 7 months does not alter brain docosahexaenoic acid content, in contrast to liver, heart and testes. Biochim. Biophy. Acta 1124, 119 - 122.Google Scholar
  13. Bourre, J.-M., Francois, M., Youyou, A., Dumont, O., Piciotti, M., Pascal, G., and Durand, G. (1989) The effects of dietary a-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 - 1892.PubMedGoogle Scholar
  14. Bowman, R. E. and Davenport, J. W. (1980) The effects of unsaturated fats upon behavior, Ann. Rep. Food Research Institute, University of Wisconsin, Madison, WI, pp. 438 440.Google Scholar
  15. Broderick, P. A., Phelan, E T., Eng, E, and Wechsler, R. T. (1994) Ibocaine modulates cocaine responses which are altered due to environmental habituation: in vivo microvoltammetric and behavioral studies. Pharmacol. Biochem. Behay. 49, 711 - 728.CrossRefGoogle Scholar
  16. Bubser, M. and Schmidt, W. J. (1990) 6-Hydroxydopamine lesion of the rat prefrontal cortex increases locomotor activity, impairs acquisition of delayed alternation tasks, but does not affect uninterrupted tasks in the radial arm maze. Behay. Brain Res. 37, 157 - 168.Google Scholar
  17. Carlson, S. E., Rhodes, P. G., and Ferguson, M. G. (1986) Docosahexaenoic acid status of preterm infants at birth and following feeding with human milk or formula. Am. J. Clin. Nutr. 44, 798 - 804.PubMedGoogle Scholar
  18. Carlson, S. E. and Werkman, S. H. (1996) A randomized trial of visual attention of preterm infants fed docosahexaenoic acid until two months. Lipids 31, 85 - 90.PubMedCrossRefGoogle Scholar
  19. Carlson, S. E., Werkman, S. H., Peeples, J. M., Cooke, R. J., and Tolley, E. A. (1993) Arachidoroic acid status correlates with first year growth in preterm infants. Proc. Natl. Acad. of Sci. USA 90, 1073 - 1077.CrossRefGoogle Scholar
  20. Carlson, S. E., Werkman, S. H., and Tolley, E. A. (1996) The effect of long chain n-3 fatty acid supplementation on visual acuity of preterm infants with and without bronchopulmonary dysplasia. Am. J. Clin. Nutr. 63, 687 - 697.PubMedGoogle Scholar
  21. Colombo, J., Mitchell, D. W., Coídren, J. T., and Freeman, L. J. (1991) Individual differences in infant visual attention: Are short lookers faster processors or feature processors? Child Dev. 62, 1247 - 1257.PubMedCrossRefGoogle Scholar
  22. Delion, S. S., Chalon, S., Herault, J., Guilloteau, D., Besnard, J.-C., and Durand, G. (1994) Chronic dietary a-linolenic acid deficiency alters dopaminergic and serotonergic neurotransmission in rats. J. Nutr. 124, 2466 - 2476.PubMedGoogle Scholar
  23. Doherty, M. and Grafton, A. (1994) Medial prefrontal cortical Dl receptors modulate stress-induced dopamine release in nucleus accumbens. Soc. Neurosci. Abs. 20, 821 (abstract).Google Scholar
  24. Dyer, J. R. and Greenwood, C. E. (1991) Neural 22-carbon fatty acids in the wean-ling rat respond rapidly and specifically to a range of dietary linoleic to a-linolenic fatty acid ratios. J. Neurochem. 56, 1921 - 1931.PubMedCrossRefGoogle Scholar
  25. Ebstein, R. P., Novick O., Umansky, R., Priel, B., Osher, Y, Blain, D., Bennett, E. R., Nemanov, L., Katz, M., and Belmaker, R. H. (1996) Dopamine D4 receptor D4DR) exon III polymorphism associated with the human personality trait of novelty seeking. Nature Genet. 12, 78 - 80.PubMedCrossRefGoogle Scholar
  26. Fagan, J. F. and Detterman, D. K. (1992) The Fagan Test of Infant Intelligence: a technical summary. J. Appl. Dev. Psychol. 13, 173 - 193.CrossRefGoogle Scholar
  27. Farquharson, J., Cockburn, F., Patrick, W. A., Jamieson, E. C., and Logan, R. W. (1992) Infant cerebral cortex phospholipid fatty-acid composition and diet. Lancet 340, 810 - 813.PubMedCrossRefGoogle Scholar
  28. File, S. E. and Wardill, A. G. (1975) Validity of head-dipping as a measure of exploration in a modified hole-board. Psychopharmacologia 44, 53 - 59.PubMedCrossRefGoogle Scholar
  29. Flood, J., Hernandez, E., and Morley, J. (1990) Memory enhancement in mice with chronic menhaden oil administration, in Geriatric Nutrition (Morley, J., Glick, Z., and Rubenstein, L.), Raven, New York, pp. 435 440.Google Scholar
  30. Forsyth, J. S. and Willets, P. (1996). Do LCPUFA influence infant cognitive behavior?, in Recent Developments in Infant Nutrition ( Bindels, J., Goedhart, A., and Visser, H., ed.), Kluwer, Lancaster, UK, pp. 225 - 234.CrossRefGoogle Scholar
  31. Foot, M., Cruz, T. F., and Clandinin, M. T. (1983) Effect of dietary lipid on synaptosomal acetylcholinesterase activity. Biochem. J. 211, 507 - 509.PubMedGoogle Scholar
  32. Francès, H., Monier, C., and Bourre, J-M. (1995) Effects of dietary a-linolenic acid deficiency on neuromuscular and cognitive function in mice. Life Sci. 57, 1935 - 1947.PubMedCrossRefGoogle Scholar
  33. Galler, J. R. and Ramsey, F. (1989) A follow-up study of the influence of early malnutrition on development: behavior at home and at school. J. Am. Acad. Child Adoles. Psychiatry 28, 254 - 261.CrossRefGoogle Scholar
  34. Gerbi, A., Zerouga, M., Debray, M., Durand, G., Chanez, C., and Bourre, J.-M. (1994) Effect of fish oil diet on fatty acid composition of phospholipids of brain membranes and on kinetic properties of Na+, K+-ATPase isoenzymes of weaned and adult rats. J. Neurochem. 62, 1560 - 1569.PubMedCrossRefGoogle Scholar
  35. Gunderson, V. M. and Sackett, G. P. (1984) Development of pattern recognition in infant pigtailed macaques (Macaca nemestrina). Dev. Psychol. 20, 418 - 426.CrossRefGoogle Scholar
  36. Hooks, M. S. and Kalivas, P. W. (1995) The role of mesoaccumbens-pallidal circuitry in novelty-induced behavioral activation. Neuroscience 64, 587 - 597.PubMedCrossRefGoogle Scholar
  37. Jacobson, S. W., Jacobson, J. L., O’Neill, J. M., Padgett, R. J., Frankowski, J. J., and Bihun, J. T. (1992) Visual expectation and dimensions of infant information processing. Child Dev. 63, 711 - 724.PubMedCrossRefGoogle Scholar
  38. Jacobson, S. W., Jacobson, J. L., Sokol, R. J., Martier, S. S., and Ager, J. W. (1993) Prenatal alcohol exposure and infant information processing ability. Child Dev. 64, 1706 - 1721.PubMedCrossRefGoogle Scholar
  39. Janowsky, J. S., Scott, D. T., Wheeler, R. E., and Auestad, N. (1995) Fatty acids affect early language development. Pediatr. Res. 37, 310A (abstract).CrossRefGoogle Scholar
  40. Johnson, M. H., Posner, M. I., and Rothbart, M. K. (1991) Components of visual orienting in early infancy: contingency learning, anticipatory looking, and disengaging. J. Cogn. Neurosci. 3, 335 - 344.CrossRefGoogle Scholar
  41. Kiyatkin, E. A. and Gratton, A. (1994) Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food. Brain Res. 652, 225 - 234.PubMedCrossRefGoogle Scholar
  42. Lamptey, M. S. and Walker, B. L. (1976) A possible essential role for dietary linolenic acid in the development of the young rat. J. Nutr. 106, 86 - 93.PubMedGoogle Scholar
  43. Levitsky, D. A. and Barnes, R. H. (1973) Malnutrition and animal behavior, in Nutrition, Development and Social Behavior (Kallen, D. J., ed.), Department of Health, Education and Welfare Publication #(NIH) 73-242, Washington DC, pp. 3-16.Google Scholar
  44. Lin, D. S., Connor, W. E., Anderson G. J., and Neuringer, M. (1990) The effect of dietary n-3 fatty acids on the phospholipid molecular species of monkey brain. J. Neurochem. 55, 1200 - 1207.PubMedCrossRefGoogle Scholar
  45. Makrides, M. and Gibson, R. A. (1995) Long-chain polyunsaturated fatty acids and visual function in infants: a current review. Br. J. Clin. Pract. Suppl. 80, 37 - 44.Google Scholar
  46. Makrides, M., Neumann, M. A., Byard, R. W., Simmer, K., and Gibson, R. A. (1994) The fatty acid composition of brain, retina, and erythrocytes in breast and formula fed infants. Am. J. Clin. Nutr. 60, 189 - 194.PubMedGoogle Scholar
  47. Makrides, M., Simmer, K., Goggin, M., and Gibson, R. A. (1993) Erythrocyte docosahexaenoic acid correlates with the visual response of healthy, term infants. Pediatr. Res. 33, 425 - 427.PubMedGoogle Scholar
  48. Mandler, J. M. (1958) Effect of early food deprivation on adult behavior in the rat. J. Comp. Physiol. Psychol. 51, 513 - 517.PubMedCrossRefGoogle Scholar
  49. McCall, R. B. and Carriger, M. S. (1993) A meta-analysis of infant habituation and recognition memory performance as predictors of later IQ. Child Dev. 64, 577 - 579.CrossRefGoogle Scholar
  50. Mitchell, J. B. and Gratton, A. (1992) Partial dopamine depletion of the prefrontal cortex leads to enhanced mesolimbic dopamine release elicited by repeated exposure to naturally reinforcing stimuli. J. Neurosci. 12, 3609 - 3618.PubMedGoogle Scholar
  51. Morgane, P., Austin-LaFrance, R., Bronzino, J., Tonkiss, J., Diaz-Cintra, S., Cintra, L., Kemper, T., and Galler, J. (1993) Prenatal malnutrition and development of the brain. Neurosci. Biobehay. Rev. 17, 91 - 128.CrossRefGoogle Scholar
  52. Nakashima, Y., Yuasa, S., Hukamizu, Y., Okuyama, H., Ohhara, T., Kameyama, T., and Nabeshima, T. (1993) Effect of a high linoleate and a high a-linolenate diet on general behavior and drug sensitivity in mice. J. Lipid Res. 34, 239 - 247.PubMedGoogle Scholar
  53. Neuringer, M., Anderson, G. J., and Connor, W. E. (1988) The essentiality of omega-3 fatty acids for the development and function of the retina and brain. Ann. Rev. Nutr. 8, 5177.CrossRefGoogle Scholar
  54. Neuringer, M., Connor, W. E., Lin, D. S., Anderson, G. J., and Barstad, L. (1991) Dietary omega-3 fatty acids: effects on retinal lipid composition and function in primates, in Retinal Degenerations ( Anderson, R. E., Hollyfield, J. G., and La Vail, M. M., eds.), CRC, New York, pp. 117 - 129.Google Scholar
  55. Neuringer, M., Connor, W., Lin, D., Barstad, L., and Luck, S. (1986). Biochemical and functional effects of prenatal and postnatal omega-3 fatty acid deficiency on retina and brain in rhesus monkey. Proc. Natl. Acad. Sci. USA 83, 4021 - 4025.PubMedCrossRefGoogle Scholar
  56. Neuringer, M., Connor, W. E., VanPetten, C., and Bartad, L. (1984) Dietary omega-3 fatty acid deficiency and visual loss in infant rhesus monkeys. J. Clin. Invest. 73, 272 - 276.PubMedCrossRefGoogle Scholar
  57. Neuringer, M., Reisbick, S., and Janowsky, J. S. (1994) The role of n-3 fatty acids in visual and cognitive development: current evidence and methods of assessment. J. Pediat. 125, S39 - S47.PubMedCrossRefGoogle Scholar
  58. Noel, B. N. and Gratton, A. (1995) Electrochemical evidence of increased dopamine transmission in prefrontal cortex and nucleus accumbens elicited by ventralGoogle Scholar
  59. tegmental µ-opioid receptor activation in freely behaving rats. Synapse 21, 110-122.Google Scholar
  60. Pita, M. L., Fernandez, M. R., De-Lucchi, C., Medina, A., Martinez-Valverde, A., Uauy, R., and Gil, A. (1988) Changes in fatty acids pattern of red blood cell phospholipid induced by type of milk, dietary nucleotide supplementation, and postnatal age in preterm infants. J. Pediatr. Gastroenterol. Nutr. 7, 740 - 747.PubMedCrossRefGoogle Scholar
  61. Ploeger, G., Spruijt, B., and Cools, A. (1994) Spatial localization in the Morris water maze in rats: Acquisition is affected by intra-accumbens injections of the dopaminergic antagonist haloperidol. Behay. Neurosci. 108, 927 - 934.CrossRefGoogle Scholar
  62. Reisbick, S., Neuringer, M., and Connor, W. (1991a) Increased repeated errors in rhesus monkeys with omega-3 fatty acid deficiency (FAD). Soc. Neurosci. Abst. 17, 1503.Google Scholar
  63. Reisbick, S., Neuringer, M., and Connor, W. E. (1996) Effects of n-3 fatty acid deficiency in nonhuman primates: implications for human infant formulas, in Recent Developments in Infant Nutrition ( Bindels, J., Goedhart, A., and Visser, H., eds.), Kluwer, Lancaster, UK, pp. 157 - 172.CrossRefGoogle Scholar
  64. Reisbick, S., Neuringer, M., Connor, W. E., and Barstad, L. (1992) Postnatal deficiency of omega-3 fatty acids in monkeys: fluid intake and urine concentration. Physiol. Behay. 51, 473 - 479.CrossRefGoogle Scholar
  65. Reisbick, S., Neuringer, M., Connor, W. E., and Iliff-Sizemore, S. (1991b) Increased intake of water and NaC1 solutions in omega-3 fatty acid deficient monkeys. Physiol. Behay. 49, 1139 - 1146.CrossRefGoogle Scholar
  66. Reisbick, S., Neuringer, M., and Gohl, E. (1994a) Increased look duration in paired comparisons by rhesus monkey infants with n-3 fatty acid deficiency. Soc. Neurosci. Abst. 20, 1696.Google Scholar
  67. Reisbick, S., Neuringer, M., Gohl, E., Wald, R., and Anderson, G. J. (1997) Visual attention in infant monkeys: effects of age and dietary fatty acids. Dev. Psychol. in press.Google Scholar
  68. Reisbick, S., Neuringer, M., Hasnain, R., and Connor, W. E. (1990) Polydipsia in rhe- sus monkeys deficient in omega-3 fatty acids. Physiol. Behay. 47, 315 - 323.CrossRefGoogle Scholar
  69. Reisbick, S., Neuringer, M., Hasnain, R., and Connor, W. E. (1994b) Home cage behavior of rhesus monkeys with long-term deficiency of omega-3 fatty acids. Physiol. Behay. 55, 231 - 239.CrossRefGoogle Scholar
  70. Roberts, H. J., Smart, J. L., and Wearden, J. H. (1982) Early life undernutrition and operant responding in the rat: the effect of the reinforcement schedule employed. Physiol. Behay. 28, 777 - 785.CrossRefGoogle Scholar
  71. Roberts, H. J., Wearden, J. H., and Smart, J. L. (1983) Undernutrition of weanling and adult rats: effects on operant responding. Behay. Brain Res. 10, 287 - 296.CrossRefGoogle Scholar
  72. Rose, S. A., Feldman, J. F., McCarton, C., and Wolfson, J. (1988) Information processing in seven-month-old infants as a function of risk status. Child Dev. 59, 589 - 603.PubMedCrossRefGoogle Scholar
  73. Salamone, J. D., Cousins, M. S., McCullough, L. D., Carriero, D. L., and Berkowitz, R. J. (1994) Nucleus accumbens dopamine relase increases during instrumental lever pressing for food but not free food consumption. Pharmacol. Biochem. Behay. 49, 25 - 31.CrossRefGoogle Scholar
  74. Sawaguchi, T. and Goldman-Rakic, P. S. (1994) The role of Dl-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of Rhesus monkeys perfoming an oculomotor delayed-response task. J. Neurophysiol. 71, 515 - 528.PubMedGoogle Scholar
  75. Smart, J. L. (1977) Early life malnutrition and later learning ability: a critical analysis, in Genetics, Environment and Intelligence ( Oliveio, A., ed.), Elsevier, North-Holland, pp. 215 - 235.Google Scholar
  76. Sokolowski, J. D., McCullough, L. D., and Salamone, J. D. (1994) Effects of dopamine depletions in the medial prefrontal cortex on active avoidance and escape in the rat. Brain Res. 651, 293 - 299.PubMedCrossRefGoogle Scholar
  77. Sokolowski, J. D. and Salamone, J. D. (1994) Effects of dopamine depletions in the medial prefrontal cortex on DRL performance and motor activity in the rat. Brain Res. 624, 20 - 28.CrossRefGoogle Scholar
  78. Stevens, L. J., Zentall, S. S., Deck, J. L., Abate, M. L., Watkins, B. A., Lipp S. R., and Burgess, J. R. (1995) Essential fatty acid metabolism in boys with attention-deficit hyperactivity disorder. J. Clin. Nutr. 62, 761 - 768.Google Scholar
  79. Thompson, L. A., Fagan, J. E, and Fulker, D. W. (1991) Longitudinal predictions of specific cognitive abilities from infant novelty preference. Child Dev. 62, 530 - 538.PubMedCrossRefGoogle Scholar
  80. Tinoco, J. (1982) Dietary requirements and function of alpha-linolenic acid in animals. Prog. Lipid Res. 21, 1 - 45.PubMedCrossRefGoogle Scholar
  81. Tonkiss, J. and Galler, J. R. (1990) Prenatal protein malnutrition and working memory performance in adult rats. Behay. Brain Res. 40, 95 - 107.CrossRefGoogle Scholar
  82. Tonkiss, J., Shukitt-Hale, B., Formica, R. N., Rocco, E J., and Galler, J. R. (1990) Prenatal protein malnutrition alters response to reward in adult rats. Physiol. Behay. 48, 675 - 680.CrossRefGoogle Scholar
  83. Tonkiss, J., Shultz, P., and Galler, J. R. (1992). Long-Evans and Sprague-Dawley rats differ in their spatial navigation performance during ontogeny and at maturity. Dev. Psychobiol. 25, 567 - 570.PubMedCrossRefGoogle Scholar
  84. Tonkiss, J., Shultz, P., and Galler, J. R. (1994) An analysis of spatial navigation in prenatally protein malnourished rats. Physiol. Behay. 55, 217 - 224.CrossRefGoogle Scholar
  85. Uauy, R. D., Hoffman, D. R., Birch, E. E., Birch, D. G., Jameson, D., and Tyson, J. (1994) Safety and efficacy of omega-3 fatty acids in the nutrition of very low birth weight infants: soy oil and marine oil supplementation of formula. J. Pediatr. 124, 612 - 620.PubMedCrossRefGoogle Scholar
  86. Wainwright, P. E. (1992) Do essential fatty acids play a role in behavioral development? Neurosci. Biobehay. Rev. 16, 193 - 205.CrossRefGoogle Scholar
  87. Wainwright, P. E., Huang, Y. S., Bulman-Fleming, B., Levesque, S., and McCutcheon, D. (1994a) The effects of dietary fatty acid composition combined with environmental enrichment on brain and behavior in mice. Behay. Brain Res. 60, 125 - 136.CrossRefGoogle Scholar
  88. Wainwright, P. E., Huang, Y-S., Bulman-Fleming, B., Mills, D. E., Redden, P., and McCutcheon, D. (1991) The role of n-3 essential fatty acids in brain and behavioral development: a cross-fostering study in the mouse. Lipids 26, 37 - 45.PubMedCrossRefGoogle Scholar
  89. Wainwright, P. E., Huang, Y. S., Coscina, D. V., Levesque, S., and McCutcheon, D. (1994b) Brain and behavioral effects of dietary n-3 deficiency in mice: a three generation study. Dev. Psychobiol. 27, 467 - 487.PubMedCrossRefGoogle Scholar
  90. Watanabe, I., Kato, M., Aonuma, H., Hashimoto, A., Naito, Y., Moriuchi, A., and Okuyama, H. (1987) Effect of dietary alpha-linolenate/linoleate balance on the lipid composition and electroretinographic response in rats. Adv. Biosci. 62, 563 - 570.Google Scholar
  91. Weidmann, T. S., Pates, R. D., Beach J. M., Salmon, A., and Brown, M. F. (1988) Lipid—protein interactions mediate the photochemical function of rhodopsin. Biochemistry 27, 6469 - 6474.CrossRefGoogle Scholar
  92. Werkman, S. H. and Carlson, S. E. (1996) A randomized trial of visual attention of preterm infants fed docosahexaenoic acid until nine months. Lipids 31, 91 - 97.PubMedCrossRefGoogle Scholar
  93. Wheeler, T. G., Benolken, R. M., and Anderson, R. E. (1975) Visual membranes: specificity of fatty acid precursors for the electrical response to illumination. Science 188, 1312 - 1314.PubMedCrossRefGoogle Scholar
  94. Williams, G. V., Rolls, E. T., Leonard, C. M., and Stern, C. (1993) Neuronal responses in the ventral striatum of the behaving macaque. Behay. Brain Res. 55, 243 - 252.CrossRefGoogle Scholar
  95. Wolterink, G., Phillips, G., Cador, M., Donselaar-Wolterink, I., Robbins, T. W., and Everitt, B. J. (1993) Relative roles of ventral striatal D1 and D2 dopamine receptors in responding with conditioned reinforcement. Psychopharmacology 110, 355 - 364.PubMedCrossRefGoogle Scholar
  96. Yamamoto, N., Hashimoto, A., Takemoto, Y., Okuyama, H., Nomura, M., Kitajima, R., Togashi, T., and Tamai, Y. (1988) Effect of the dietary a-linolenate/linoleate balance on lipid compositions and learning ability of rats. II. Discrimination process, extinction process, and glycolipid compositions. J. Lipid Res. 29, 1013 - 1021.PubMedGoogle Scholar
  97. Yamamoto, N., Okaniwa, Y., Mori, S., Nomura, N., and Okuyama, H. (1991) Effects of a high-linoleate and a high-a-linolenate diet on the learning ability of aged rats. J. Gerontol. Biol. Sci. 46, B17 - 22.Google Scholar
  98. Yamamoto, N., Saitoh, M., Moriuchi, A., Nomura, M., and Okuyama, H. (1987) Effect of dietary a-linolenate/linoleate balance on brain lipid compositions and learning ability of rats. J. Lipid Res. 28, 143 - 150.Google Scholar
  99. Yeaton, S. P., O’Connell, M. F., and Strobel, D. A. (1978) Malnutrition and social isolation: Learning in the developing Rhesus monkey. Physiol. Behay. 20, 125 – 128.CrossRefGoogle Scholar
  100. Yehuda, S. and Carasso, R. L. (1993) Modulation of learning, pain thresholds, and thermoregulation in the rat by preparations of free purified a-linolenic and linoleic acids: determination of the optimal w3-to-w6 ratio. Proc. Natl. Acad. Sci. USA 90, 10345 - 10349.PubMedCrossRefGoogle Scholar
  101. Yehuda, S., Leprohon-Greenwood, C. E., Dixon, L. M., and Cosina, D. V. (1986) Effects of dietary fat on pain threshold, thermoregulation and motor activity in rats. Pharmacol. Biochem. Behay. 24, 1775 - 1777.CrossRefGoogle Scholar
  102. 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. Biosci. Biotechnol. Biochem. 57, 253 - 259.CrossRefGoogle Scholar

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© Springer Science+Business Media New York 1997

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  • Sydney Reisbick
  • Martha Neuringer

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