Long-Chain Polyunsaturated Fatty Acids in Human Brain Evolution

Human Brain Evolution: The Influence of Freshwater and Marine Food Resources

Volumn , Issue , 2010, Pages 13-31

  Crawford, Michael A ^a  

^a LONDON METROPOLITAN UNIVERSITY   (United Kingdom)

Author keywords

Docosahexaenoic acid (DHA) major PUFA constituent of brain; Evolution of complex life forms Darwin's view, "natural selection and conditions of existence"; Long chain polyunsaturated fatty acids in human brain evolution

Indexed keywords

EID: 80051767860     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470609880.ch2     Document Type: Chapter

References (86)

1. Allwood, A.C., Walter, M.R., Kamber, B.S., Marshall, C.P., and Burch, I.W. 2006. Stromatolite reef from the Early Archaean era of Australia. Nature 441: 714-718.
2. Anderle, P., Farmer, P., Berger, A., and Roberts, M.A. 2004. Nutrigenomic approach to understanding the mechanisms by which dietary long chain fatty acids induce gene signals and control mechanisms involved in carcinogenesis. Nutrition 20: 103-108.
3. Anderson, R.E. and Maude, M.B. 1972. Lipids of ocular tissues: The effects of essential fatty acid deficiency on the phospholipids of the photoreceptor membranes of rat retina. Arch Biochem Biophys 151: 270-276.
4. Andlin-Sobocki, P., Jonsson, J., Wittchen, H.-U., and Olesen, J. 2005. Cost of disorders of the brain in Europe. Eur J Neurol 12 (Suppl. 1): 1-27.
5. Barcelo Coblijn, G., Hogyes, E., Kitajka, K., Puskas, L.G., Zvara, A., Hackler, L. Jr., Nyakas, C., Penke, Z., and Farkas, T. 2003a. Modification by docosahexaenoic acid of age-induced alterations in gene expression and molecular composition of rat brain phospholipids. Proc Natl Acad Sci U S A 100: 11321-11326.
6. Barcelo Coblijn, G., Kitajka, K., Puskas, L.G., Hogyes, E., Zvara, A., Hackler, L. Jr., and Farkas, T. 2003b. 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: 72-79.
7. Barker, D.J. 2004. The developmental origins of chronic adult disease. Acta Paediatr Suppl 93 (446): 26-33.
8. Bazan, N.G. 2007. Homeostatic regulation of photoreceptor cell integrity: Significance of the potent mediator neuroprotectin D1 biosynthesized from docosahexaenoic acid. The Proctor Lecture. Invest Ophthalmol Vis Sci 48 (11): 4866-4881.
9. Benolken, R.M., Anderson, R.E., and Wheeler, T.G. 1973. Membrane fatty acids associated with the electrical response in visual excitation. Science 182 (118): 1253-1254.
10. Birch, E.E., Garfield, S., Hoffman, D.E., Hoffman, D.R., Uauy, R., and Birch, D.G. 2000. A randomised trial of early dietary supply of long chain polyunsaturated fatty acids and mental development in term infants. Dev Med Child Neurol 42: 174-181.
11. Bitsanis, D., Crawford, M.A., Moodley, T., Holmsen, H., Ghebremeskel, K., and Djahanbakhch, O. 2005. AA predominates in the membrane phosphoglycerides of the early and term human placenta. J Nutr 135 (11): 2566-2571.
12. Bloom, M., Linseisen, F., Lloyd-Smith, J., and Crawford, M.A. 1999. Insights from NMR on the functional role of polyunsaturated lipids in the brain. Magnetic Resonance and Brain Function-Approaches from Physics, ed. B. Maraviglia. Proceedings of the 1998 Enrico Fermi International School of Physics, Enrico Fermi Lecture, Course #139, Varenna, Italy, pp. 1-27.
13. Bourre, J.M., Francois, M., Youyou, A., Dumont, O., Piciotti, M., Pascal, G., and Durand, G. 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 (12): 1880-1892.
14. Bramble, D. and Lieberman, D. 2004. Endurance running and the evolution of Homo. Nature 432: 345-352.
15. Broadhurst, C.L., Wang, Y., Crawford, M.A., Cunnane, S., Parkington, J., and Schmid, W.F. 2002. Brain-specific lipids from marine, lacustrine, or terrestrial food resources: Potential impact on early African Homo sapiens. Comp Biochem Physiol B Biochem Mol Biol 131: 653-673.
16. Budowski, P. and Crawford, M.A. 1985. Alpha-linolenic acid as a regulator of the metabolism of AA: Dietary implications of the ratio n-6:n-3 fatty acids. Proc Nutr Soc 44: 221-229.
17. Budowski, P., Leighfield, M.J., and Crawford, M.A. 1987. Nutritional encephalomalacia in the chick: An exposure of the vulnerable period for cerebellar development and the possible need for both ? 6 and ? 3 fatty acids. Br J Nutr 58: 511-520.
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.
19. Catalan, J., Moriguchi, T., Slotnick, B., Murthy, M., Greiner, R.S., and Salem, N. Jr. 2002. Cognitive deficits in docosahexaenoic acid-deficient rats. Behav Neurosci 116: 1022-1031, 2078S-2083S.
20. Chawla, A., Repa, J.J., Evans, R.M., and Mangelsdorf, D.J. 2001. Nuclear receptors and lipid physiology: Opening the X-files. Science 294 (5548): 1866-1870.
21. Chung, W.L., Chen, J.J., and Su, H.M. 2008. Fish oil supplementation of control and (n-3) fatty acid-deficient male rats enhances reference and working memory performance and increases brain regional docosahexaenoic acid levels. J Nutr 138 (6): 1165-1167.
22. Chytrova, G., Ying, Z., and Gomez-Pinilla, F. 2009. Exercise contributes to the effects of DHA dietary supplementation by acting on membrane-related synaptic systems. Brain Res May 13, ahead of publication at time of submission.
23. Corella, D. and Ordovas, J.M. 2005. Single nucleotide polymorphisms that influence lipid metabolism: Interaction with dietary factors. Annu Rev Nutr 25: 341-390.
24. Crawford, M.A. 1971. Epidemiological interactions. In Symposium on Mycotoxins in Human Health, ed. I.F.H. Purchase, pp. 231-244. Proceedings of a Symposium in Pretoria, 1970. London: Macmillan.
25. Crawford, M.A., Bloom, M., Broadhurst, C.L., Schmidt, W.F., Cunnane, S.C., Galli, C., Ghebremeskel, K., Linseisen, F., Lloyd-Smith, J., and Parkington, J. 1999. Evidence for the unique function of DHA during the evolution of the modern hominid brain. Lipids 34: S39-S47.
26. Crawford, M.A., Broadhurst, C.L., Galli, C., Ghebremeskel, K., Holmsen, H., Saugstad, L.F., Schmidt, F., Sinclair, A.J., and Cunnane, S.C. 2008. The role of docosahexaenoic and AAs as determinants of evolution and hominid brain development. In Fisheries for Global Welfare and Environment, ed. K. Tsukamoto, T. Kawamura, T. Takeuchi, T.D. Beard Jr., and M.J. Kaiser, pp. 57-76. 5th World Fisheries Congress 2008, Terrapub, Tokyo.
27. Crawford, M.A., Casperd, N.M., and Sinclair, A.J. 1976. The long chain metabolites of linoleic and linolenic acids in liver and brain in herbivores and carnivores. Comp Biochem Physiol 54B: 395-401.
28. Crawford, M.A., Cunnane, S.C., and Harbige, L.S. 1993. A new theory of evolution: Quantum theory. IIIrd International Congress on Essential Fatty Acids and Eicosanoids. American Oil Chemists Society, ed A.J. Sinclair and R. Gibson. Adelaide, pp. 87-95.
29. Crawford, M.A., Gale, M.M., and Woodford, M.H. 1969. Linoleic acid and linolenic acid elongation products in muscle tissue of Syncerus caffer and other ruminant species. Biochem J 115: 25-27.
30. Crawford, M.A., Golfetto, I., Bistanis, D., Ghebremeskel, K., Min, Y., Moodley, T., Poston, L., Phylactos, A., Cunnane, S., and Schmidt, W. 2003. Arachidonic and docosahexaenoic acids in protection against central nervous system damage in preterm infants. Lipids 38 (4): 303-315.
31. Crawford, M.A. and Marsh, D.E. 1995. Nutrition and Evolution: Food in Evolution and the Future. New Canaan, CT: Keats.
32. Crawford, M.A. and Sinclair, A.J. 1972. Nutritional influences in the evolution of the mammalian brain. In Lipids, Malnutrition and Developing Brain, ed. K. Elliot and J. Knight, pp. 267-292. A Ciba Foundation Symposium. Amsterdam: Elsevier.
33. Cunnane, S.C. 2005. Survival of the Fattest: The Key to Human Brain Evolution, River Edge, NJ: World Scientific Publishing.
34. Darwin, C. 1868. The Origin of Species by Means of Natural Selection. Or the Preservation of Favoured Races in the Struggle for Life. London: John Murray.
35. Dawkins, C.R. 1999. The Selfish Gene. Oxford University Press.
36. Eldridge, N. and Gould, S.J. 1972. Punctuated equilibria: an alternative to phyletic gradualism. In T.J.M. Schopf, ed., Models in Paleobiology. San Francisco, CA: Freeman, Cooper, pp. 82-115.
37. Fiennes, R.N.T.-W., Sinclair, A.J., and Crawford, M.A. 1973. Essential fatty acid studies in primates: Linolenic acid requirements of Capuchins. J Med Primatol 2: 155-169.
38. Freemantle, E., Tremblay, S., Vandal, M., Tremblay-Mercier, J., Blachère, J.C., Bégin, M.E., Windust, T., Brenna, J.T., and Cunnane, S.C. 2006. Omega-3 fatty acids, energy substrates and brain function during aging. Prostagl Leukotri Essential Fatty Acids 75: 213-220.
39. Galli, C. and Socini, A. 1983. Dietary lipids in pre-and post-natal development. In Dietary Fats and Health, ed. E.G. Perkins and W.J. Visek, pp. 278-301. Champaign, IL: American Oil Chemists Society.
40. Gislén, A., Dacke, M., Kröger, R.H., Abrahamsson, M.,Nilsson, D.E., and Warrant, E.J. 2003. Superior underwater vision in a human population of sea gypsies. Curr Biol 13 (10): 833-836.
41. Hardy, A. 1960. Was man more aquatic in the past? The New Scientist, March 17, pp. 642-645.
42. Hibbeln, J.R. 2002. Seafood consumption, the DHA content of mothers' milk and prevalence rates of postpartum depression: A cross-national, ecological analysis. J Affect Disord 69 (1-3): 15-29.
43. Hibbeln, J.R. 2007. From homicide to happiness-A commentary on omega-3 fatty acids in human society. Cleave Award Lecture. Nutr Health 19 (1-2): 9-19.
44. Hibbeln, J.R., Davis, J., Steer, C., Emmett, P., Rogers, I., Williams, C., and Golding, J. 2007. Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): An observational cohort study. Lancet 369 (9561): 578-585.
45. Hibbeln, J.R., Nieminen, L.R., and Lands, W.E. 2004. Increasing homicide rates and linoleic acid consumption among five Western countries, 1961-2000. Lipids 39 (12): 1207-1213.
46. Hindenes, J.O., Nerdal, W., Guo, W., Di, L., Small, D.M., and Holmsen, H. 2000. Physical properties of the transmembrane signal molecule, sn-1-stearoyl 2-arachidonoylglycerol. Acyl chain segregation and its biochemical implications. J Biol Chem 275 (10): 6857-6867.
47. Holland, H.D. 2006. The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci 361 (1470): 903-915.
48. James, M.J. and Cleland, L.G. 2004. Applying a research ethics committee approach to a medical practice controversy: The case of the selective COX-2 inhibitor rofecoxib. J Med Ethics 30: 182-184.
49. Jump, D.B. 2002. The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem 277 (11): 8755-8758.
50. Kitajka, K., Puskas, L.G., Zvara, A., Hackler, L. Jr., Barcelo Coblijn, G., Yeo, Y.K., and Farkas, T. 2002. The role of n-3 polyunsaturated fatty acids in brain: Modulation of rat brain gene expression by dietary n-3 fatty acids. Proc Natl Acad Sci U S A 99: 2619-2624.
51. Kitajka, K., Sinclair, A.J., Weisinger, R.S., Weisinger, H.S., Mathai, M., Jayasooriya, A.P., Halver, J.E., and Puskas, L.G. 2004. Effects of dietary omega-3 polyunsaturated fatty acids on brain gene expression. Proc Natl Acad Sci U S A 101: 10931-10936.
52. Lagarde, M., Bernoud, N., Brossard, N., Lemaitre-Delaunay, D., Thies, F., Croset, M., and Lecerf, J. 2001. Lysophosphatidylcholine as a preferred carrier form of docosahexaenoic acid to the brain. J Mol Neurosci 16 (2-3): 201-204 ; discussion 215-221.
53. 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 (1): 86-93.
54. Leaf, A.A., Leighfield, M.J., Costeloe, K.L., and Crawford, M.A. 1992. Factors affecting long-chain polyunsaturated fatty acid composition of plasma choline phosphoglycerides in preterm infants. J Pediatr Gastroenterol Nutr 14: 300-308.
55. Leyton, J., Drury, P.J., and Crawford, M.A. 1987. Differential oxidation of saturated and unsaturated fatty acids in vivo in the rat. Br J Nutr 57: 383-393.
56. Marean, C.W., Bar-Matthews, M., Bernatchez, J., Fisher, E., Goldberg, P., Herries, A.I., Jacobs, Z., Jerardino, A., Karkanas, P., Minichillo, T., Nilssen, P.J., Thompson, E., Watts, I., and Williams, H.M. 2007. Early human use of marine resources and pigment in South Africa during the Middle Pleistocene. Nature 449 (7164): 905-908.
57. Martinez, M. and Vazquez, E. 1998. MRI evidence that docosahexaenoic acid ethyl ester improves myelination in generalized peroxisomal disorders. Neurology 51 (1): 26-32.
58. Morgan, E. 1995. The Descent of the Child. Oxford: Oxford University Press.
59. Morgan, E. 1997. The Aquatic Ape Hypothesis. London: Souvenir Press.
60. Neuringer, M., Connor, W.E., Lin, D.S., 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 monkeys. Proc Natl Acad Sci U S A 83 (11): 4021-4025.
61. Otsuka, J. 2008. Theoretical approach to the large-scale evolution of multicellularity and cell differentiation. J Theor Biol 255 (1): 129-136.
62. Pauletto, P., Puato, M., Caroli, M.G., Casiglia, E., Munhambo, A.E., Cazzolato, G., Bon, G.B., Angeli, M.T., Galli, C., and Pessina, A.C. 1996. Blood pressure and atherogenic lipoprotein profiles of fish-diet and vegetarian villagers in Tanzania: The Lugalawa study. Lancet 348: 784-788.
63. Plourde, M. and Cunnane, S.C. 2007. Extremely limited conversion of long chain omega 3 polyunsaturates in adults: Implications for their dietary essentiality and use as supplements. Appl Physiol Nutr Metab 32: 619-634.
64. Ray, W.A., Stein, C.M., Daugherty, J.R. Hall, K., Arbogast, P.G., and Griffin, M.R. 2002. COX-2 selective non-steroidal anti-inflammatory drugs and risk of serious coronary heart disease. Lancet 360: 1071-1073.
65. Rivers, J.P.W., Sinclair, A.J., and Crawford, M.A. 1975. Inability of the cat to desaturate essential fatty acids. Nature 285: 171-173.
66. Rodriguez de Turco, E.B., Gordon, W.C., and Bazan, N.G. 1992. Light stimulates in vivo inositol lipid turnover in frog retinal pigment epithelial cells at the onset of shedding and phagocytosis of photoreceptor membranes. Exp Eye Res 55: 719-725.
67. Ruyle, M., Connor, W.E., Anderson, G.J., and Lowensohn, R.I. 1990. Placental transfer of essential fatty acids in humans: Venous-arterial difference for docosahexaenoic acid in fetal umbilical erythrocytes. Proc Natl Acad Sci U S A 87 (20): 7902-7906.
68. Serhan, C.N., Chiang, N., and Van Dyke, T.E. 2008. Resolving inflammation: Dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8 (5): 349-361.
69. Sinclair, A.J. 1975. Incorporation of radioactive polyunsaturated fatty acids into liver and brain of developing rat. Lipids 10 (3): 175-184.
70. Sinclair, A.J. and Crawford, M.A. 1972. The incorporation of linolenic and docosahexaenoic acid into liver and brain lipids of developing rats. FEBS Lett 26: 127-129.
71. Smit, E.N., Muskiet, F.A., and Boersma, E.R. 2004. The possible role of essential fatty acids in the pathophysiology of malnutrition. Prostaglandins Leukot Essent Fatty Acids 71 (4): 241-250.
72. Sprecher, H. 1993. Interconversions between 20-and 22-carbon n-3 and n-6 fatty acids via 4-desaturase independant pathways. IIIrd International Congress on Essential Fatty Acids and Eicosanoids. American Oil Chemists Society, ed. A.J. Sinclair and R. Gibson. Adelaide, pp. 18-22.
73. Sprecher, H., Chen, Q., and Yin, F.Q. 1999. Regulation of the biosynthesis of 22:5n-6 and 22:6n-3: A complex intracellular process. Lipids 34: S153-S156.
74. Stein, A.D., Zybert, P.A., van der Pal-de Bruin, K., and Lumey, L.H. 2006. Exposure to famine during gestation, size at birth, and blood pressure at age 59 y: Evidence from the Dutch famine. Eur J Epidemiol 21 (10): 759-765.
75. Steinberg, G., Slaton, W.H. Jr., Howton, D.R., and Mead, J.F. 1956. Metabolism of essential fatty acids. IV. Incorporation of linoleate into AA. J Biol Chem 220 (1): 257-264.
76. Stringer, C. 2000. Palaeoanthropology. Coasting out of Africa. Nature 405 (6782): 24-25, 27.
77. Suzuki, H., Manabe, S., Wada, O., and Crawford, M.A. 1997. Rapid incorporation of docosahexaenoic acid from dietary sources into brain microsomal, synaptosomal and mitochondrial membranes in adult mice. Internat J Vit Res 67: 272-278.
78. Tobias, P.V. 1998. Water and human evolution. Out There 35: 38-44.
79. Ward, P. 2009. What will become of Homo sapiens? Sci Am 300: 68-73.
80. Weisinger, H.S., Vingrys, A.J., Bui, B.V., and Sinclair, A.J. 1999. Effects of dietary n-3 fatty acid deficiency and repletion in the guinea pig retina. Invest Ophthalmol Vis Sci 40: 327-338.
81. Weismann, A. 1893. The all-sufficiency of natural selection. Contemp Rev 64: 309-338, 596-610.
82. 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.
83. Wiegand, R.D., Koutz, C.A., Chen, H., and Anderson, R.E. 1995. Effect of dietary fat and environmental lighting on the phospholipid molecular species of rat photoreceptor membranes. Exp Eye Res 60 (3): 291-306.
84. Williams, G. and Crawford, M.A. 1987. Comparison of the fatty acid component in structural lipids from dolphins, zebra and giraffe: Possible evolutionary implications. J Zool Lond 213: 673-684.
85. Yamamoto, N., Okaniwa, Y., Mori, S., Nomura, M., and Okuyama, H. 1991. Effects of a high-linoleate and a high-alpha-linolenate diet on the learning ability of aged rats. Evidence against an autoxidation-related lipid peroxide theory of aging. J Gerontol 46 (1): B17-B22.
86. Yavin, E., Himovichi, E., and Eilam, R. 2009. Delayed cell migration in the developing rat brain following maternal omega 3 alpha linolenic acid dietary deficiency. Neuroscience 162: 1011-1022.