Advertisement

Lipids

, Volume 36, Issue 9, pp 885–895 | Cite as

Essential fatty acids in visual and brain development

  • Ricardo UauyEmail author
  • Dennis R. Hoffman
  • Patricio Peirano
  • David G. Birch
  • Eileen E. Birch
Article

Abstract

Essential fatty acids are structural components of all tissues and are indispensable for cell membrane synthesis; the brain, retina and other neural tissues are particularly rich in long-chain polyunsaturated fatty acids (LC-PUFA). These fatty acids serve as specific precursors for eicosanoids, which regulate numerous cell and organ functions. Recent human studies support the essential nature of n-3 fatty acids in addition to the well-established role of n−6 essential fatty acids in humans, particularly in early life. The main findings are that light sensitivity of retinal rod photoreceptors is significantly reduced in newborns with n−3 fatty acid deficiency, and that docosahexaenoic acid (DHA) significantly enhances visual acuity maturation and cognitive functions. DHA is a conditionally essential nutrient for adequate neurodevelopment in humans. Comprehensive clinical studies have shown that dietary supplementation with marine oil or single-cell oil sources of LC-PUFA results in increased blood levels of DHA and arachidonic acid, as well as an associated improvement in visual function in formula-fed infants matching that of human breast-fed infants. The effect is mediated not only by the known effects on membrane biophysical properties, neurotransmitter content, and the corresponding electrophysiological correlates but also by a modulating gene expression of the developing retina and brain. Intracellular fatty acids or their metabolites regulate transcriptional activation of gene expression during adipocyte differentiation and retinal and nervous system development. Regulation of gene expression by LC-PUFA occurs at the transcriptional level and may be mediated by nuclear transcription factors activated by fatty acids. These nuclear receptors are part of the family of steroid hormone receptors. DHA also has significant effects on photoreceptor membranes and neurotransmitters involved in the signal transduction process; rhodopsin activation, rod and cone development, neuronal dendritic connectivity, and functional maturation of the central nervous system.

Keywords

Visual Acuity Essential Fatty Acid Term Infant Chain Polyunsaturated Fatty Acid Mental Development Index 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AA

arachidonic acid (20∶4n−6)

ABER

auditory brainstemevoked response

ALA

α-linolenic acid (18∶3n−3)

CNS

central nervous system

DHA

docosahexaenoic acid (22∶6n−3)

EFA

essential fatty acid

ERG

electroretinogram

FA

fatty acids

FPL

forced-choice preferential looking

GLA

γ-linolenic acid (18∶3n−6)

LA

linoleic acid (18∶2n−6)

LC-PUFA

long-chain polyunsaturated fatty acids

MI

metarhodopsin I

M II

metarhodopsin II

MDI

Mental Development Index

PC

phosphatidylcholine

PPAR

peroxisome proliferator-activated receptor

PUFA

polyunsaturated fatty acid

RBC

red blood cell

RxR

retinoic acid receptor

TR

thyroxine receptor

VEP

visual-evoked potential

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Dobbing, J., Hopewell, J.W., and Lynch, A. (1971) Vulnerability of Developing Brain. VII. Permanent Deficit of Neurons in Cerebral and Cerebellar Cortex Following Early Mild Undernutrition, Exp. Neurol. 32, 439–447.PubMedCrossRefGoogle Scholar
  2. 2.
    Pollitt, E. (1988) A Critical View of Three Decades of Research on the Effects of Chronic Energy Undernutrition on Behavioral Development, in Chronic Energy Deficiency, (Schurch, B., and Scrimshaw, N., eds.), IDECG, Lausanne Switzerland.Google Scholar
  3. 3.
    Fagioli, I., Peirano, P., Bes, F., and Salzarulo, P. (1989) Sleep in Early Human Malnutrition, in Sleep '88, (Horne, J.A., ed.), pp. 58–62, Gustav Fischer Verlag, Stuttgart.Google Scholar
  4. 4.
    Spassov, L., Curzi-Dascalova, L., Clairambault, J., Kauffmann, F., Eiselt, M., Médigue, C., and Peirano, P. (1994) Heart Rate and Heart Rate Variability During Sleep in Small-for-Gestational Age Newborns, Pediatr. Res. 35, 500–505.PubMedGoogle Scholar
  5. 5.
    Grantham-McGregor, S. (1995) A Review of Studies of the Effect of Severe Malnutrition on Mental Development, J. Nutr. 125, 2233S-2238S.PubMedGoogle Scholar
  6. 6.
    Uauy, R., Birch, D.G., Birch, E.E., Tyson, J.E., and Hoffman, D.R. (1990) Effect of Dietary Omega-3 Fatty Acids on Retinal Function of Very Low Birth Weight Neonates, Pediatr. Res. 28, 485–492.PubMedGoogle Scholar
  7. 7.
    Birch, E.E., Birch, D.G., and Hoffman, D.R. (1992) 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
  8. 8.
    Birch, E.E., Birch, D.G., Hoffman, D.R., and Uauy, R.D. (1992) Dietary Essential Fatty Acid Supply and Visual Acuity Development, Invest. Ophthalmol. Vis. Sci. 33, 3242–3253.PubMedGoogle Scholar
  9. 9.
    Carlson, S.E., Werkman, S.H., Rhodes, P.G., and Tolley, E.A. (1993) Visual-Acuity Development in Healthy Preterm Infants: Effect of Marine-Oil Supplementation, Am. J. Clin. Nutr. 58, 35–42.PubMedGoogle Scholar
  10. 10.
    Carlson, S.E., Werkman, S.H., Peeples, J.M., and Wilson, W.M., III (1994) Growth and Development of Premature Infants in Relation to ω-3 and ω-6 Fatty Acid Status, World Rev. Nutr. Diet. 75, 63–69.PubMedGoogle Scholar
  11. 11.
    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, 85–91.PubMedCrossRefGoogle Scholar
  12. 12.
    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
  13. 13.
    Carlson, S.E., Werkman, S.H., and Tolley, E.A. (1996) Effect of Long Chain n−3 Fatty Acid Supplementation on Visual Acuity and Growth of Preterm Infants With and Without Bronchopulmonary Dysplasia, Am. J. Clin. Nutr. 63, 687–697.PubMedGoogle Scholar
  14. 14.
    Faldella, G., Govoni, M., Alessandroni, R., Marchiani, E., Salvioli, G.P., Biagi, P.L., and Spano, C. (1996) Visual Evoked Potentials and Dietary Long Chain Polyunsaturated Fatty Acids in Preterm Infants, Arch. Dis. Child. 75, F108-F112.Google Scholar
  15. 15.
    O'Connor, D.L., Hall, R., Adamkin, D., Auestad, N., Castillo, M., Connor, W.E., Connor, S.L., Fitzgerald, K., Groh-Wargo, S., Hartmann, E.E., et al. (2001) Growth and Development in Preterm Infants Fed Long-Chain Polyunsaturated Fatty Acids: A Prospective, Randomized Control Trial, Pediatrics 108, 359–371.PubMedCrossRefGoogle Scholar
  16. 16.
    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
  17. 17.
    Bjerve, K.S., Brubakk, A.M., Fougner, K.J., Johnsen, H., Midthjell, K., and Vik, T. (1993) Omega-3 Fatty Acids: Essential Fatty Acids with Important Biological Effects, and Serum Phospholipid Fatty Acids as Markers of Dietary Omega-3 Fatty Acid Intake, Am. J. Clin. Nutr. 57, 801S-806S.PubMedGoogle Scholar
  18. 18.
    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. 34, 425–427.CrossRefGoogle Scholar
  19. 19.
    Courage, M.L., McCloy, U.R., Herzberg, G.R., Andrews, W.L., Simmons, B.S., McDonald, A.C., Mercer, C.N., and Friel, J.K. (1998) Visual Acuity Development and Fatty Acid Composition of Erythrocytes in Full-Term Infants Fed Breast Milk, Commercial Formula, or Evaporated Milk, J. Dev. Behav. Pediatr. 19, 9–17.PubMedGoogle Scholar
  20. 20.
    Jorgensen, M.H., Hernell, O., Lund, P., Holmer, G., and Michaelsen, K.F. (1996) Visual Acuity and Erythrocyte Docosahexaenoic Acid Status in Breast-Fed and Formula-Fed Term Infants During the First Four Months of Life, Lipids 31, 99–105.PubMedCrossRefGoogle Scholar
  21. 21.
    Innis, S., Nelson, C., Lwanga, D., Rioux, F.M., and Waslen, P. (1996) Feeding Formula Without Arachidonic Acid and Docosahexaenoic Acid Has No Effect on Preferential Looking Acuity or Recognition Memory in Healthy Full-Term Infants at 9 Months of Age, Am. J. Clin. Nutr. 64, 40–46.PubMedGoogle Scholar
  22. 22.
    Innis, S.M., Nelson, C.M., Rioux, M.F., and King, D.J. (1994) Development of Visual Acuity in Relation to Plasma and Erythrocyte ω-6 and ω-3 Fatty Acids in Healthy Term Gestation Infants, Am. J. Clin. Nutr. 60, 347–352.PubMedGoogle Scholar
  23. 23.
    Innis, S.M., Akrabawi, S., Diersen-Schade, D., Dobson, M.V., and Guy, D.G. (1997) Visual Acuity and Blood Lipids in Term Infants Fed Human Milk or Formulae, Lipids 32, 63–72.PubMedCrossRefGoogle Scholar
  24. 24.
    Jensen, C., Prager, T., Fraley, J., Chen, H., Anderson, R., and Heird, W. (1997) Functional Effects of Dietary Linoleic/Linolenic Acid Ratio in Term Infants, J. Pediatr. 130, 200–204.Google Scholar
  25. 25.
    Makrides, M., Neumann, M., Simmer, K., Pater, J., and Gibson, R. (1995) Are Long-Chain Polyunsaturated Fatty Acids Essential Nutrients in Infancy? Lancet 345, 1463–1468.PubMedCrossRefGoogle Scholar
  26. 26.
    Carlson, S.E., Ford, A.J., Werkman, S.H., Peeples, J.M., and Koo, W.W. (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, 882–888.PubMedGoogle Scholar
  27. 27.
    Jorgensen, H.M., Holmer, G., Lund, P., Hernell, O., and Michaelsen, K.F. (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, 412–421.CrossRefGoogle Scholar
  28. 28.
    Auestad, N., Montalto, M., Hill, R., Fitzgerald, K.M., Wheeler, R.E., Connor, W.E., Neuringer, M., Connor, S.L., Taylor, J.A., and Hartmann, E.E. (1997) Visual Acuity, Erythrocyte Fatty Acid Composition, and Growth in Term Infants Fed Formulas with Long Chain Polyunsaturated Fatty Acid for One Year, Pediatr. Res. 41, 1–10.PubMedGoogle Scholar
  29. 29.
    Scott, D.T., Janowsky, J.S., Hall, R.T., Carroll, R.E., Taylor, J.A., Auestad, N., and Montalto, M.B. (1998) Formula Supplementation with Long-Chain Polyunsaturated Fatty Acids: Are There Developmental Benefits? Pediatrics 102, E59.PubMedCrossRefGoogle Scholar
  30. 30.
    Agostoni, C., Trojan, S., Bellu, R., Riva, E., and Giovannini, M. (1995) Neurodevelopmental Quotient of Healthy Term Infants at 4 Months and Feeding Practice: The Role of Long Chain Polyunsaturated Fatty Acids, Pediatr. Res. 38, 262–266.PubMedGoogle Scholar
  31. 31.
    Agostoni, C., Trojan, S., Bellu, R., Riva, E., Bruzzese, M.G., and Giovannini, M. (1997) Developmental Quotient at 24 Months and Fatty Acid Composition of Diet in Early Infancy: A Follow-Up Study, Arch. Dis. Child. 76, 421–424.PubMedCrossRefGoogle Scholar
  32. 32.
    Gibson, R., Neumann, M., and Makrides, M. (1997) Effect of Increasing Breast Milk Docosahexaenoic Acid on Plasma and Erythrocyte Phospholipid Fatty Acids and Neural Indices of Exclusively Breast-Fed Infants, Eur. J. Clin. Nutr. 51, 578–584.PubMedCrossRefGoogle Scholar
  33. 33.
    Birch, E.E., Hoffman, D.R., Uauy, R., Birch, D.G., and Prestidge, C. (1998) Visual Acuity and the Essentiality of Docosahexaenoic Acid and Arachidonic Acid in the Diet of Term Infants, Pediatr. Res. 44, 201–209.PubMedGoogle Scholar
  34. 34.
    Birch, E.E., Garfield, S., Hoffman, D.R., Uauy, R., and Birch, D.G. (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, 174–181.PubMedCrossRefGoogle Scholar
  35. 35.
    Forsyth, J.S., and Willatts, P. (1996) Do LC-PUFA Influence Infant Cognitive Behavior? in Recent Developments in Infant Nutrition (Bindles, J.G., Goedhart, A.C., and Visser, H.K., eds.), pp. 225–234, Kluwer Academic Publishers, London.Google Scholar
  36. 36.
    Willatts, P., Forsyth, J.S., DiModugno, M.K., Varma, S., and Colvin, M. (1998) Effect of Long Chain Polyunsaturated Fatty Acids in Infant Formula on Problem Solving at 10 Months of Age [comment], Lancet 352, 688–691.PubMedCrossRefGoogle Scholar
  37. 37.
    Slater, A. (1995) Individual Differences in Infancy and Later IQ, J. Child Psychol. Psychiatry 36, 69–112.PubMedGoogle Scholar
  38. 38.
    Lucas, A., Stafford, M., Morley, R., Abbott, R., Stephenson, T., MacFayden, U., Elias-Jones, A., and Clements, H. (1999) Efficacy and Safety of Long-Chain Polyunsaturated Fatty Acid Supplementation of Infant-Formula Milk: A Randomised Trial, Lancet 354, 1948–1954.PubMedCrossRefGoogle Scholar
  39. 39.
    Gibson, R. (1999) Long-Chain Polyunsaturated Fatty Acids and Infant Development, Lancet 354, 1919–1920.PubMedCrossRefGoogle Scholar
  40. 40.
    Makrides, M., Neumann, A., Simmer, K., and Gibson, R.A. (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, 32–38.PubMedCrossRefGoogle Scholar
  41. 41.
    San Giovanni, J.P., Parra-Cabrera, S., Colditz, G.A., Berkey, C.S., and Dwyer, J.T. (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, 1292–1298.CrossRefGoogle Scholar
  42. 42.
    San Giovanni, J.P., Berkey, C.S., Dwyer, J.T., and Colditz, G.A. (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, 165–188.CrossRefGoogle Scholar
  43. 43.
    Cousins, R. (1994) Metal Elements and Gene Expression, Annu. Rev. Nutr. 14, 449–469.PubMedCrossRefGoogle Scholar
  44. 44.
    Clarke, S.D., and Jump, D.D. (1994) Dietary Polyunsaturated Fatty Acid Regulation of Gene Transcription, Annu. Rev. Nutr. 14, 83–98.PubMedCrossRefGoogle Scholar
  45. 45.
    Gottlicher, M., Demoz, A., Svenson, D., Tollet, P., Berge, R.K., and Gustaffson, J.A. (1993) Structural and Metabolic Requirements for Activators of the Peroxisome Proliferator-Activated Receptor, Biochem. Pharmacol. 46, 2177–2184.PubMedCrossRefGoogle Scholar
  46. 46.
    Rotstein, N.P., Politi, L.E., and Aveldaño, M.I. (1998) Docosahexaenoic Acid Promotes Differentiation of Developing Photoreceptors in Culture, Invest. Ophthalmol. Vis. Sci. 39, 2750–2758.PubMedGoogle Scholar
  47. 47.
    Rodriguez de Turco, E.B., Deretic, D., Bazan, N.G., and Papermaster, D.S. (1997) Post Golgi Vesicles Cotransport Docosahexaenoyl Phospholipids and Rhodopsin During Frog Photoreceptor Membranes Biogenesis, J. Biol. Chem. 272, 10494–10497.Google Scholar
  48. 48.
    Dreyer, C., Keller, H., Mahfaudi, A., Laudet, V., Krey, G., and Wahli, W. (1993) Positive Regulation of the Peroxisomal Beta-Oxidation Pathway by Fatty Acids Through Activation of Peroxisome Proliferator-Activated Receptor (PPAR), Biol. Cell 77, 67–76.PubMedCrossRefGoogle Scholar
  49. 49.
    Yu, K., Bayona, W., Kallen, C.B., Harding, H.P., Ravera, C.P., MacMahon, G., Brown, M., and Lazar, M.A. (1995) Differential Activation of Peroxisome Proliferator Activated Receptor by Eicosanoids, J. Biol. Chem. 270, 23975–23983.PubMedCrossRefGoogle Scholar
  50. 50.
    Kersten, S., Desvergne, B., and Wahli, W. (2000) Roles of PPARs in Health and Disease, Nature 405, 421–424.PubMedCrossRefGoogle Scholar
  51. 51.
    Wheeler, T., Benolken, R., and Anderson, R. (1997) Visual Membranes: Specificity of Fatty Acid Precursors for the Electrical Response to Illumination, Science 188, 1312–1314.CrossRefGoogle Scholar
  52. 52.
    Stubbs, C., and Smith, A. (1984) The Modification of Mammalian Membrane Polyunsaturated Fatty Acid Composition in Relation to Membrane Fluidity and Function, Biochim. Biophys. Acta 779, 89–137.PubMedGoogle Scholar
  53. 53.
    Lee, A., East, J., and Froud, R. (1986) Are Essential Fatty Acids Essential for Membrane Function?, Prog. Lipid Res. 25, 41–46.PubMedCrossRefGoogle Scholar
  54. 54.
    Treen, M., Uauy, R., Jameson, D., Thomas, V., and Hoffman, D. (1992) Effect of Docosahexaenoic Acid on Membrane Fluidity and Function in Intact Cultured Y-79 Retinoblastoma Cells, Arch. Biophys. 294, 564–570.CrossRefGoogle Scholar
  55. 55.
    Lin, D., Connor, W., Anderson, G., and Neuringer, M. (1990) Effects of Dietary n−3 Fatty Acids on the Phospholipid Molecular Species of Monkey Brain, J. Neurochem. 55, 1200–1207.PubMedCrossRefGoogle Scholar
  56. 56.
    Litman, B., and Mitchell, D. (1996) A Role for Phospholipid Polyunsaturation in Modulating Membrane Protein Function, Lipids 31, S193-S197.PubMedCrossRefGoogle Scholar
  57. 57.
    Weidmann, T., Pates, R., Beach, J., Salmon, A., and Brown, M. (1988) Lipid-Protein Interactions Mediate the Photochemical Function of Rhodopsin, Biochemistry 27, 6469–6474.CrossRefGoogle Scholar
  58. 58.
    Mitchell, D., Straume, M., and Litman, B. (1992) Role of sn-1-Saturated, sn-2-Polyunsaturated Phospholipids in Control of Membrane Receptor Conformational Equilibrium: Effects of Cholesterol and Acyl Chain Unsaturation on the Metarhodopsin I in Equilibrium with Metarhodopsin II, Biochemistry 31, 662–670.PubMedCrossRefGoogle Scholar
  59. 59.
    Love, J., Saurn, W., and McGee, R. (1985) The Effects of Exposure to Exogenous Fatty Acids and Membrane Fatty Acid Modification on the Electrical Properties of NG108-15 Cells, Cell. Mol. Neurobiol. 5, 333–352.PubMedCrossRefGoogle Scholar
  60. 60.
    Vreugdenhil, M., Bruehl, C., Voskuyl, R., Kang, J., Leaf, A., and Wadman, W. (1996) Polyunsaturated Fatty Acids Modulate Sodium and Calcium Currents in CA1 Neurons, Proc. Natl. Acad. Sci. USA 93, 12559–12563.PubMedCrossRefGoogle Scholar
  61. 61.
    Weylandt, K., Kang, J., and Leaf, A. (1996) Polyunsaturated Fatty Acids Exert Anti-Arrhythmic Actions as Free Acids Rather than in Phospholipids, Lipids 31, 977–982.PubMedCrossRefGoogle Scholar
  62. 62.
    Voskuyl, R., Vreugdenhil, M., Kang, J., and Leaf, A. (1998) Anticonvulsant Effect of Polyunsaturated Fatty Acids in Rats. Using the Cortical Stimulation Model, Eur. J. Pharmacol. 341, 145–152.PubMedCrossRefGoogle Scholar
  63. 63.
    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
  64. 64.
    Neuringer, M., Connor, W.E., Van Petten, C., and Barstad, L. (1984) Dietary Omega-3 Fatty Acid Deficiency and Visual Loss in Infant Rhesus Monkeys, J. Clin. Investig. 73, 272–276.PubMedCrossRefGoogle Scholar
  65. 65.
    Hubel, D., and Wiesel, T. (1970) The Period of Susceptibility to the Physiological Effects of Unilateral Eye Closure in Kittens, J. Physiol. 206, 419–436.PubMedGoogle Scholar
  66. 66.
    Hubel, D.H., and Wiesel, T.N. (1977) Plasticity of Ocular Dominance Columns in Monkey Striate Cortex, Phil. Trans. R. Soc. Lond. B Biol. Sci. 278, 377–409.Google Scholar
  67. 67.
    Jameson, L., and Caplow, M. (1981) Modification of Microtubule Steady-State Dynamics by Phosphorylation of the Microtubule-Associated Proteins, Proc. Natl. Acad. Sci. USA 78, 3413–3417.PubMedCrossRefGoogle Scholar
  68. 68.
    Aoki, C., and Siekevitz, P. (1985) Ontogenetic Changes in the Cyclic Adenosine 3′,5′-Monophosphate-Stimulatable Phosphorylation of Cat Visual Cortex Proteins, Particularly of Microtubule-Associated Protein 2 (MAP 2): Effects of Normal and Dark Rearing and of the Exposure to Light, J. Neurosci. 5, 2465–2483.PubMedGoogle Scholar
  69. 69.
    Bornstein, M.H. (1989) Sensitive Periods in Development: Structural Characteristics and Causal Interpretations, Psychol. Bull. 105, 179–197.PubMedCrossRefGoogle Scholar
  70. 70.
    Blakemore, C. (1991) Sensitive and Vulnerable Periods in the Development of the Visual System, in The Childhood Environment and Adult Disease, (Bock, G.R., and Whelan, J., eds.) pp. 129–154, Ciba Foundation Symposium, John Wiley & Sons, Chichester.Google Scholar
  71. 71.
    Williams, C., Birch, E.E., Emmet, P., North, K., and ALSPAC Team (2001) Stereoacuity at 3.5 Years of Age 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, 316–322.PubMedGoogle Scholar

Copyright information

© AOCS Press 2001

Authors and Affiliations

  • Ricardo Uauy
    • 1
    • 2
    Email author
  • Dennis R. Hoffman
    • 2
  • Patricio Peirano
    • 1
  • David G. Birch
    • 2
  • Eileen E. Birch
    • 2
  1. 1.Institute of Nutrition and Food Technology (INTA)University of ChileSantiagoChile
  2. 2.Retina Foundation of the SouthwestDallas

Personalised recommendations