Skip to content
Frontiers
Search

Neuroscience

Frontiers in Evolutionary Neuroscience ·

Volume 3 - 2011 | https://doi.org/10.3389/fnevo.2011.00005

Sex Differences in the Relationship of Dietary Fatty Acids to Cognitive Measures in American Children

  • William D. Lassek1,2*corresponding author
  • Steven J. C. Gaulin2
  1. 11 Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh Pittsburgh, PA, USA
  2. 22 Department or Anthropology, University of California Santa Barbara, CA, USA
Article metrics0 viewsView details
PDFCiteMetrics

Abstract

Because the first neurons evolved in an environment high in the n −3 (omega-3) fatty acid docosahexaenoic acid (DHA), this fatty acid became a major component of neural structure and function and makes up 10% of the dry weight of the human brain. Since n −3 fatty acids must come from the diet, this suggests a possible positive role for dietary n −3 fatty acids in cognition and a possible negative role for n −6 fatty acids, which compete with n −3 for access to critical enzymes. Because human females must provide DHA for the growth of the unusually large brains of their offspring from maternal fat stored during childhood, their need for DHA is especially great. We used stepwise regression to determine whether particular dietary fatty acids and other nutrients were related to cognitive performance in over 4000 American children aged 6–16 from the Third National Health and Nutrition Examination Survey; a variety of possible biological, social, and environmental risk factors were statistically controlled. In this context the only dietary factors related to cognitive performance were n −3 and n −6 fatty acids. Dietary n −3 fatty acids were positively related to cognitive test scores in male and female children, while n −6 showed the reverse relationship, significantly so in females. In female children the positive effects of n −3 intake were twice as strong as in males and exceeded the negative effects of lead exposure. This suggests that increasing dietary intake of n −3 and decreasing n −6 fatty acids may have cognitive benefits in children, especially in females.

Keywords

References

  1. Aberg M. A. L., Aberg N., Brisman J., Sundberg R., Winkvist A., Toren K. (2009). Fish intake of Swedish male adolescents is a predictor of cognitive performance. Acta Paediatr. 98, 555 – 560. doi:10.1111/j.1651-2227.2008.01103.x
  2. Agostoni C., Trojan S., Bell R., Riva E., Bruzzese M. G., 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. doi:10.1136/adc.76.5.421
  3. Ahmad A., Moriguchi T., Salem N. (2002). Decrease in neuron size in docosahexaenoic acid-deficient brain. Pediatr. Neurol. 26, 210 – 218. doi:10.1016/S0887-8994(01)00383-6
  4. Arija V., Esparo G., Fernandez-Ballart J., Murphy M. M., Biarnes E., Canals J. (2006). Nutritional status and performance in test of verbal and non-verbal intelligence in 6 year old children. Intelligence 34, 141 – 149. doi:10.1016/j.intell.2005.09.001
  5. Auestad N., Innis S. M. (2000). Dietary n-3 fatty acid restriction during gestation in rats: neuronal cell body and growth-cone fatty acids. Am. J. Clin. Nutr. 71, 312S – 314S.
  6. Beltz B. S., Tlusty M. F., Benton J. L., Sandeman D. C. (2007). Omega-3 fatty acids upregulate adult neurogenesis. Neurosci. Lett. 415, 154 – 158. doi:10.1016/j.neulet.2007.01.010
  7. Blasbalg T. L., Hibbeln J. R., Ramsden C. E., Majchrzak S. F., Rawlings R. R. (2011). Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am. J. Clin. Nutr. 93, 950 – 962. doi:10.3945/ajcn.110.006643
  8. Bongiovanni K. D., Depeters E. J., Van Eenennaam A. L. (2007). Neonatal growth rate and development of mice raised on milk transgenically enriched with omega-3 fatty acids. Pediatr. Res. 62, 412 – 416.
  9. Boot A. M., Bouquet J., Ridder M. A. J. D., Krenning E. P., Keizer-Shrama S. M. (1997). Determinants of body composition measured by dual-energy x-ray absorptiometry in Dutch children and adolescents. Am. J. Clin. Nutr. 66, 232 – 238.
  10. Bourre J. M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G., 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, 1880 – 1892.
  11. Brand M. D., Couture P., Else P. L., Withers K. W., Hulbert A. J. (1991). Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem. J. 275, 81 – 86.
  12. Brand M. D., Couture P., Hulbert A. J. (1994). Liposomes from mammalian liver mitochondria are more polyunsaturated and leakier to protons than those from reptiles. Comp. Biochem. Physiol. Biochem. Mol. Biol. 108, 181 – 188. doi:10.1016/0305-0491(94)90064-7
  13. Braun D. R., Harris J. W. K., Levin N. E., Mccoy J. T., Herries A. I. R., Bamford M. K., Bishop L. C., Richmond B. G., Kibunjia M. (2010). Early hominin diet included diverse terrestrial and aquatic animals 1.95 Ma in East Turkana, Kenya. Proc. Natl. Acad. Sci. U.S.A. 107, 10002 – 10007. doi:10.1073/pnas.1002181107
  14. Broadhurst C. L., Wang Y., Crawford M. A., Cunnane S. C., Parkington J. E., Schmidt 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. 131B, 653 – 673. doi:10.1016/S1096-4959(02)00002-7
  15. Calderon F., Kim H.-Y. (2004). Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J. Neurochem. 90, 979 – 988. doi:10.1111/j.1471-4159.2004.02808.x
  16. Cansev M., Wurtman R. J. (2007). Chronic administration of docosahexaenoic acid or eicosapentaenoic acid, but not arachidonic acid, alone or in combination with uridine, increases brain phosphatide and synaptic protein levels in gerbils. Neuroscience 148, 421 – 431. doi:10.1016/j.neuroscience.2007.06.016
  17. Cao D., Kevala K., Kim J., Moon H.-S., Jun S. B., Lovinger D., Kim H.-Y. (2009). Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J. Neurochem. 111, 510 – 521. doi:10.1111/j.1471-4159.2009.06300.x
  18. Chang C.-Y., Ke D.-S., Chen J.-Y. (2009). Essential fatty acids and human brain. Acta Neurol. Taiwan. 18, 231 – 241.
  19. Chung W. L., Chen J. J., 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, 1165 – 1171.
  20. Clandinin M. T., Chappell J. E., Leong S., Heim T., Swyer P. R., Chance G. W. (1980a). Extrauterine fatty acid accretion in infant brain: implications for fatty acid requirements. Early Hum. Dev. 4, 131 – 138. doi:10.1016/0378-3782(80)90016-X
  21. Clandinin M. T., Chappell J. E., Leong S., Heim T., Swyer R., Chance G. W. (1980b). Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Hum. Dev. 4, 121 – 129. doi:10.1016/0378-3782(80)90016-X
  22. Clutton-Brock T. H., Harvey P. H. (1980). Primates, brains and ecology. J. Zool. (Lond.) 190, 309 – 323. doi:10.1111/j.1469-7998.1980.tb01430.x
  23. Cockburn F. (1994). Neonatal brain and dietary lipids. Arch. Dis. Child. 70, F1 – F2. doi:10.1136/adc.70.5.369
  24. Coluccia A., Borracci P., Renna G., Giustino A., Latronico T., Riccio P., Carratu M. R. (2009). Developmental omega-3 supplementation improves motor skills in juvenile-adult rats. Int. J. Dev. Neurosci. 27, 599 – 605. doi:10.1016/j.ijdevneu.2009.05.011
  25. Coti Bertrand P., O’usky J. R., Innis S. M. (2006). Maternal dietary (n-3) fatty acid deficiency alters neurogenesis in the embryonic rat brain. J. Nutr. 136, 1570 – 1575.
  26. Da Costa K.-A., Rai K. S., Craciunescu C. N., Parikh K., Mehedint M. G., Sanders L. M., Mclean-Pottinger A., Zeisel S. H. (2009). Dietary docosahexaenoic acid supplementation modulates hippocampal development in the Pemt-/- mouse. J. Biol. Chem. 285, 1008 – 1015. doi:10.1074/jbc.M109.017137
  27. Dagai L., Peri-Naor R., Birk R. (2009). Docosahexaenoic acid significantly stimulates immediate early response genes and neurite outgrowth. Neurochem. Res. 34, 867 – 875. doi:10.1007/s11064-008-9845-z
  28. Dalton A., Wolmarans P., Witthuhn R. C., Van Stuijvenberg M. E., Swanevelder S. A., Smuts C. M. (2009). A randomised control trial in schoolchildren showed improvement in cognitive function after consuming a bread spread, containing fish flour from a marine source. Prostaglandins Leukot. Essent. Fatty Acids 80, 143 – 149. doi:10.1016/j.plefa.2008.12.006
  29. De Groot R. H., Hornstra G., Jolles J. (2007). Exploratory study into the relation between plasma phospholipid fatty acid status and cognitive performance. Prostaglandins Leukot. Essent. Fatty Acids 76, 165 – 172. doi:10.1016/j.plefa.2007.01.001
  30. Eilander A., Hundscheid D. C., Osendarp S. J., Transler C., Zock P. L. (2007). Effects of n-3 long chain polyunsaturated fatty acid supplementation on visual and cognitive development throughout childhood: a review of human studies. Prostaglandins Leukot. Essent. Fatty Acids 76, 189 – 203. doi:10.1016/j.plefa.2007.01.003
  31. Emken E. A., Adlof R. O., Gulley R. M. (1994). Dietary linoleic acid influences desaturation and acylation of deuterium-labeled linoleic and linolenic acids in young males. Biochim. Biophys. Acta 1213, 277 – 288.
  32. Fedorova I., Hussein N., Baumann M. H., Di Martino C., Salem N. Jr. (2009). An n-3 fatty acid deficiency impairs rat spatial learning in the Barnes maze. Behav. Neurosci. 123, 196 – 205. doi:10.1037/a0013801
  33. Fontaneto D., Tommaseo-Ponzetta M., Galli C., Risé P., Glew R. H., Paoletti M. G. (2011). Differences in fatty acid composition between aquatic and terrestrial insects used as food in human nutrition. Ecol. Food Nutr. 50, 351 – 367. doi:10.1080/03670244.2011.586316
  34. Garcia-Calatayud S., Redondo C., Martin E., Ruiz J. I., Garcia-Fuentes M., Sanjurjo P. (2005). Brain docosahexaenoic acid status and learning in young rats submitted to dietary long-chain polyunsaturated fatty acid deficiency and supplementation limited to lactation. Pediatr. Res. 57, 719 – 723. doi:10.1203/01.PDR.0000156506.03057.AD
  35. Gerrior S., Bente L., Hiza H. (2004). Nutrient content of the US food supply, 1909–2000 (Home Economics Res. Report Number 56). USDA Center for Nutrition Policy and Promotion, Alexandria.
  36. Gibson R. A., Muhlhausler B., Makrides M., Gibson R. A., Muhlhausler B., Makrides M. (2011). Conversion of linoleic acid and alpha-linolenic acid to long-chain polyunsaturated fatty acids (LCPUFAs), with a focus on pregnancy, lactation and the first 2 years of life. Matern. Child Nutr. 7 (Suppl. 2), 17 – 26. doi:10.1111/j.1740-8709.2011.00299.x
  37. Greiner R. S., Moriguchi T., Hutton A., Slotnick B. M., Salem N. Jr. (1999). Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids 34 (Suppl.), S239 – S243. doi:10.1007/BF02562305
  38. Haggarty P. (2004). Effect of placental function on fatty acid requirements during pregnancy. Eur. J. Clin. Nutr. 58, 1559 – 1570. doi:10.1038/sj.ejcn.1602016
  39. Harnack K., Andersen G., Somoza1 V. (2009). Quantitation of alpha-linolenic acid elongation to eicosapentaenoic and docosahexaenoic acid as affected by the ratio of n6/n3 fatty acids. Nutr. Metab. (Lond.) 6, 8. doi:10.1186/1743-7075-6-8
  40. Harvey P. H., Clutton-Brock T. H., Mace G. M. (1980). Brain size and ecology in small mammals and primates. Proc. Natl. Acad. Sci. U.S.A. 77, 4387 – 4389. doi:10.1073/pnas.77.7.4387
  41. He C., Qu X., Cui L., Wang J., Kang J. X. (2009). Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proc. Natl. Acad. Sci. U.S.A. 106, 11370 – 11375. doi:10.1073/pnas.0906923106
  42. Heinemann K. M., Bauer J. E. (2006). Docosahexaenoic acid and neurologic development in animals. J. Am. Vet. Med. Assoc. 228, 700 – 705. doi:10.2460/javma.228.5.700
  43. Hibbeln J. R., Nieminen L. R. G., Blasbalg T. L., Riggs J. A., Lands W. E. M. (2006). Healthy intakes of n-3 and n-6 fatty acids: estimations considering worldwide diversity. Am. J. Clin. Nutr. 83, 1483S – 1493S.
  44. Holguin S., Huang Y., Liu J., Wurtman R. (2008). Chronic administration of DHA and UMP improves the impaired memory of environmentally impoverished rats. Behav. Brain Res. 191, 11 – 16. doi:10.1016/j.bbr.2008.02.042
  45. Holman R. T. (1998). The slow discovery of the importance of omega-3 essential fatty acids in human health. J. Nutr. 128, 427s – 433s.
  46. Hooijmans C. R., Van Der Zee C. E., Dederen P. J., Brouwer K. M., Reijmer Y. D., Van Groen T., Broersen L. M., Lutjohann D., Heerschap A., Kiliaan A. J., Van Der Zee C. E. E. M. (2009). DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPswe/PS1dE9 mice. Neurobiol. Dis. 33, 482 – 498. doi:10.1016/j.nbd.2008.12.002
  47. Hulbert A. J. (2007). Membrane fatty acids as pacemakers of animal metabolism. Lipids 42, 811 – 819. doi:10.1007/s11745-007-3058-0
  48. Innis S. M. (2009). Omega-3 fatty acids and neural development to 2 years of age: do we know enough for dietary recommendations? J. Pediatr. Gastroenterol. Nutr. 48 (Suppl. 1), S16 – S24. doi:10.1097/MPG.0b013e31819773cf
  49. Innis S. M., Vaghri Z., King D. J. (2004). N-6 docosapentaenoic acid is not a predictor of low docosahexaenoic acid status in Canadian school children. Am. J. Clin. Nutr. 80, 768 – 773.
  50. Issa A. M., Moijica W. A., Morton S. C., Traina S., Newberry S. J., Hilton L. G., Garland R. H., Maclean C. H. (2006). The efficacy of omega-3 fatty acids on cognitive function in aging and dementia: a systematic review. Dement. Geriatr. Cogn. Disord. 21, 88 – 96. doi:10.1159/000090224
  51. Jamieson E. C., Farquharson J., Logan R. W., Howatson A. G., Patrick W. J. A., Weaver L. T., Cockburn F. (1999). Infant cerebellar gray and white matter fatty acids in relation to age and diet. Lipids 34, 1065 – 1071. doi:10.1007/s11745-999-0458-5
  52. Javaux E. J., Marshall C. P., Bekker A. (2010). Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463, 934 – 938. doi:10.1038/nature08793
  53. Jerde R. S., Joel P., Stroemer J., Haight R., Joel C. (1975). Comparison of nervous-tissue lipid fatty acid patterns of various animal species with particular reference to docosahexaenoic acid. Biochem. Soc. Trans. 3, 727 – 730.
  54. Jiang L.-H., Shi Y., Wang L.-S., Yang Z.-R. (2009). The influence of orally administered docosahexaenoic acid on cognitive ability in aged mice. J. Nutr. Biochem. 20, 735 – 741. doi:10.1016/j.jnutbio.2008.08.004
  55. Kennedy D. O., Jackson P. A., Elliott J. M., Scholey A. B., Robertson B. C., Greer J., Tiplady B., Buchanan T., Haskell C. F., Kennedy D. O., Jackson P. A., Elliott J. M., Scholey A. B., Robertson B. C., Greer J., Tiplady B., Buchanan T., Haskell C. F. (2009). Cognitive and mood effects of 8 weeks’ supplementation with 400 mg or 1000 mg of the omega-3 essential fatty acid docosahexaenoic acid (DHA) in healthy children aged 10–12 years. Nutr. Neurosci. 12, 48 – 56. doi:10.1179/147683009X388887
  56. Kirby A., Woodward A., Jackson S., Wang Y., Crawford M. A. (2010). Childrens’ learning and behaviour and the association with cheek cell polyunsaturated fatty acid levels. Res. Dev. Disabil. 31, 731 – 742. doi:10.1016/j.ridd.2009.08.010
  57. Kitajka K., Puskas L. G., Zvara A., Hackler L. H. Jr., Barcelo-Coblijn G., Yoo Y. K., 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. doi:10.1073/pnas.042698699
  58. Knutsen S. F., Fraser G. E., Beeson W. L., Lindsted K. D., Shavlik D. J. (2003). Comparison of adipose tissue fatty acids with dietary fatty acids as measured by 24-hour recall and food frequency questionnaire in black and white Adventists: the Adventist Health Study. Ann. Epidemiol. 13, 119 – 127. doi:10.1016/S1047-2797(02)00260-0
  59. Koletzko B., Cetin I., Brenna J. T. (2007). Dietary fat intakes for pregnant and lactating women. Br. J. Nutr. 98, 873 – 877. doi:10.1017/S0007114507764747
  60. Korn E. L., Graubard B. I. (1991). Epidemiologic studies utilizing surveys: accounting for the sampling design. Am. J. Public Health 81, 1166 – 1173. doi:10.2105/AJPH.81.9.1166
  61. Kuipers R. S., Luxwold M. F., Dijck-Brouwer D. A. J., Eaton S. B., Crawford M. A., Cordain L., Muskiet F. A. J. (2010). Estimated macronutrient and fatty acid intakes from an East African Paleolithic diet. Br. J. Nutr. 104, 1666 – 1687. doi:10.1017/S0007114510002679
  62. Kumosani T. A., Moselhy S. S., Kumosani T. A., Moselhy S. S. (2011). Modulatory effect of cod-liver oil on Na(+)-K(+) ATPase in rats’ brain. Hum. Exp. Toxicol. 30, 267 – 274. doi:10.1177/0960327110371699
  63. Lassek W. D., Gaulin S. J. C. (2006). Changes in body fat distribution in relation to parity in American women: a covert form of maternal depletion. Am. J. Phys. Anthropol. 131, 295 – 302. doi:10.1002/ajpa.20394
  64. Lassek W. D., Gaulin S. J. C. (2007). Menarche is related to fat distribution. Am. J. Phys. Anthropol. 133, 1147 – 1151. doi:10.1002/ajpa.20644
  65. Lassek W. D., Gaulin S. J. C. (2008). Waist-hip ratio and cognitive ability: is gluteofemoral fat a privileged store? Evol. Hum. Behav. 29, 26 – 34. doi:10.1016/j.evolhumbehav.2007.07.005
  66. Lim S.-Y., Hoshiba J., Moriguchi T., Salem N. Jr. (2005). N-3 fatty acid deficiency induced by a modified artificial rearing method leads to poorer performance in spatial learning tasks. Pediatr. Res. 58, 741 – 748. doi:10.1203/01.PDR.0000180547.46725.CC
  67. Liu J.-W., Almaguel F. G., Bu L., De Leon D. D., De Leon M. (2008). Expression of E-FABP in PC12 cells increases neurite extension during differentiation: involvement of n-3 and n-6 fatty acids. J. Neurochem. 106, 2015 – 2029. doi:10.1111/j.1471-4159.2008.05411.x
  68. McCann J. C., Ames B. N. (2005). 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. Am. J. Clin. Nutr. 82, 281 – 295.
  69. McGrew W. C. (1979). “Evolutionary implications of sex differences in chimpanzee predation and tool use,” in The Great Apes, eds Hamburg D. A., McCown E. R. (London: Benjamin Cummings), 441 – 463.
  70. Mitchell T. W., Ekroos K., Blanksby S. J., Hulbert A. J., Else P. L. (2007). Differences in membrane acyl phospholipid composition between an endothermic mammal and an ectothermic reptile are not limited to any phospholipid class. J. Exp. Biol. 210, 3440 – 3450. doi:10.1242/jeb.007286
  71. Mukherjee P. K., Chawla A., Loayza M. S., Bazan N. G. (2007). Docosanoids are multifunctional regulators of neural cell integrity and fate: significance in aging and disease. Prostaglandins Leukot. Essent. Fatty Acids 77, 233 – 238. doi:10.1016/j.plefa.2007.10.022
  72. NCES. (2005). Highlights From the Trends in International Mathematics, and Science Study: TIMSS. (2003). Department of Education, National Center for Educational Statistics, 2005–2005, Washington, DC.
  73. Needleman H. L., Landrigan P. J. (2004). What level of lead in blood is toxic for a child? Am. J. Public Health 94, 8. doi:10.2105/AJPH.94.1.8-a
  74. Neggers Y. H., Kim E.-K., Song J.-M., Chung E.-J., Um Y.-S., Park T. (2009). Mental retardation is associated with plasma omega-3 fatty acid levels and the omega-3/omega-6 ratio in children. Asia Pac. J. Clin. Nutr. 18, 22 – 28.
  75. Nichols P. D., Danaher K. T., Koslow J. A. (2003). Occurrence of high levels of tetracosahexaenoic acid in the jellyfish Aurelia sp. Lipids 11, 1207 – 1210. doi:10.1007/s11745-003-1180-z
  76. Niemoller T. D., Stark D. T., Bazan N. G. (2009). Omega-3 fatty acid docosahexaenoic acid is the precursor of neuroprotectin D1 in the nervous system. World Rev. Nutr. Diet. 99, 46 – 54. doi:10.1159/000192994
  77. Novak E. M., Dyer R. A., Innis S. M. (2008). High dietary omega-6 fatty acids contribute to reduced docosahexaenoic acid in the developing brain and inhibit secondary neurite growth. Brain Res. 1237, 136 – 145. doi:10.1016/j.brainres.2008.07.107
  78. Osendarp S. J., Baghurst K. I., Bryan J., Calvaresi E., Hughes D., Hussaini M. (2007). Effect of a 12-mo micronutrient intervention on learning and memory in well-nourished and marginally nourished school-aged children: 2 parallel, randomized, placebo-controlled studies in Australia and Indonesia. Am. J. Clin. Nutr. 86, 1082 – 1093.
  79. Ouellet M., Emond V., Chen C., Julien C., Bourasset F., Oddo S., Laferla F., Bazinet R. P., Calon F. (2009). Diffusion of docosahexaenoic and eicosapentaenoic acids through the blood-brain barrier: an in situ cerebral perfusion study. Neurochem. Int. 55, 476. doi:10.1016/j.neuint.2009.04.018
  80. Pawlosky R. J., Hibbeln J. R., Novotny J. A., Salem N. (2001). Physiological compartmental analysis of alpha-linolenic acid metabolism in adult humans. J. Lipid Res. 42, 1257 – 1265.
  81. Pifferi F., Jouin M., Alessandri J. M., Haedke U., Roux F., Perriere N., Denis I., Lavialle M., Guesnet P. (2007). N-3 fatty acids modulate brain glucose transport in endothelial cells of the blood-brain barrier. Prostaglandins Leukot. Essent. Fatty Acids 77, 279 – 286. doi:10.1016/j.plefa.2007.10.011
  82. Plomin R., DeFries J. C., McClearn G. E., McGuffin P. (2000). Behavioral Genetics, 4th Edn. New York: Worth.
  83. Pond C. M., Mattacks C. A. (1987). The anatomy of adipose tissue in captive Macaca monkeys and its implications for human biology. Folia Primatol. (Basel) 48, 164 – 185. doi:10.1159/000156293
  84. Putnam J., Allshouse J., Kantor L. S. (2002). U.S. per capita food supply trends: more calories, refined carbohydrates, and fats. Food Rev. 25, 1 – 15.
  85. Putnam N. H., Srivastava M., Hellsten U., Dirks B., Chapman J., Salamov A., Terry A., Shapiro H., Lindquist E., Kapitonov V. V., Jurka J., Genikhovich G., Grigoriev I. V., Lucas S. M., Steele R. E., Finnerty J. R., Technau U., Martindale M. Q., Rokhsar D. S. (2007). Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86 – 94. doi:10.1126/science.1139158
  86. Rapoport S. I. (2003). In vivo approaches to quantifying and imaging brain arachidonic and docosahexaenoic acid metabolism. J. Pediatr. 143, S26 – S34. doi:10.1016/S0022-3476(03)00182-3
  87. Redford K. H., Bouchardet Da Fonseca G. A., Lacher T. E. J. (1984). The relationship between frugivory and insectivory in primates. Primates 25, 433 – 440. doi:10.1007/BF02381666
  88. Richardson A. J., Montgomery P. (2005). The Oxford-Durham Study: a randomized, controlled trial of dietary supplementation with fatty acids in children with developmental coordination disorder. Pediatrics 115, 1360 – 1366. doi:10.1542/peds.2004-2164
  89. Rubin D., Laposata M. (1992). Cellular interactions between n-6 and n-3 fatty acids: a mass analysis of fatty acid elongation/desaturation, distribution among complex lipids, and conversion to eicosanoids. J. Lipid Res. 33, 1431 – 1440.
  90. Ryan A. S., Astwood J. D., Gautier S., Kuratko C. N., Nelson E. B., Salem N. Jr. (2010). Effects of long-chain polyunsaturated fatty acid supplementation on neurodevelopment in childhood: a review of human studies. Prostaglandins Leukot. Essent. Fatty Acids 82, 305 – 314. doi:10.1016/j.plefa.2010.02.007
  91. Ryan A. S., Nelson E. B. (2008). Assessing the effect of docosahexaenoic acid on cognitive functions in healthy, preschool children: a randomized, placebo-controlled, double-blind study. Clin. Pediatr. (Phila) 47, 355 – 362. doi:10.1177/0009922807311730
  92. Sakamoto T., Cansev M., Wurtman R. J. (2007). Oral supplementation with docosahexaenoic acid and uridine-5 ′ -monophosphate increases dendritic spine density in adult gerbil hippocampus. Brain Res. 1182, 50 – 59. doi:10.1016/j.brainres.2007.08.089
  93. Salem N. Jr., Moriguchi T., Greiner R. S., Mcbride K., Ahmad A., Catalan J. N., Slotnick B. (2001). Alterations in brain function after loss of docosahexaenoate due to dietary restriction of n-3 fatty acids. J. Mol. Neurosci. 16, 299 – 307. doi:10.1385/JMN:16:2-3:299
  94. Sauerwald T. U., Demmelmair H., Fidler N., Koletzko B. (2000). Polyunsaturated fatty acid supply with human milk. Adv. Exp. Med. Biol. 478, 261 – 270.
  95. Schuchardt J. P., Huss M., Stauss-Grabo M., Hahn A. (2010). Significance of long-chain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children. Eur. J. Pediatr. 169, 149 – 164. doi:10.1007/s00431-009-1035-8
  96. Sekula W., Nelson M., Figurska K., Oltarzewski M., Weisell R., Szponar L. (2005). Comparison between household budget survey and 24-hour recall data in a nationally representative sample of Polish households. Public Health Nutr. 8, 430 – 439. doi:10.1079/PHN2004695
  97. Shanker K., Shireesha K. K. S., Kumar S. V., Srinivas C., Rao J. V., Prasad R. B. (2006). Isolation and characterization of neutral lipids of desilked eri silkworm pupae grown on castor and tapioca leaves. J. Agric. Food Chem. 2006, 3305 – 3309. doi:10.1021/jf060581x
  98. Shirai N., Suzuki H. (2004). Effect of dietary docosahexaenoic acid and catechins on maze behavior in mice. Ann. Nutr. Metab. 48, 51 – 58. doi:10.1159/000075305
  99. Simopoulos A. P., Leaf A., Salem N. S. Jr. (1999). Workshop on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids. J. Am. Coll. Nutr. 18, 487 – 489.
  100. Slater B., Enes C. C., Lopez R. V., Damasceno N. R., Voci S. M., Slater B., Enes C. C., Lopez R. V. M., Damasceno N. R. T., Voci S. M. (2010). Validation of a food frequency questionnaire to assess the consumption of carotenoids, fruits and vegetables among adolescents: the method of triads. Cad. Saude Publica 26, 2090 – 2100. doi:10.1590/S0102-311X2010001100010
  101. Stark W. S., Lin T. N., Brackhahn D., Christianson J. S., Sun G. Y. (1993). Fatty acids in the lipids of Drosophila heads: effects of visual mutants, carotenoid deprivation and dietary fatty acids. Lipids 28, 345 – 350. doi:10.1007/BF02536355
  102. Stewart K. M. (2010). “The case for exploitation of wetlands by pre-sapiens hominins,” in Human Brain Evolution: The Influence of Freshwater and Marine Food Resources, eds Cunnane S. C., Stewart K. M. (Hoboken: John Wiley and Sons), 137 – 172.
  103. Stoknes I. S., Økland H. M. W., Falch E., Synnes M. (2004). Fatty acid and lipid class composition in eyes and brain from teleosts and elasmobranchs. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 138, 183 – 191. doi:10.1016/j.cbpc.2004.03.009
  104. Svennerholm L. (1968). Distribution and fatty acid composition of phosphoglycerides in normal human brain. J. Lipid Res. 9, 570 – 579.
  105. Takeuchi T., Fukumoto Y., Harada E. (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 – 203. doi:10.1016/S0166-4328(01)00392-8
  106. Turner N., Else P. L., Hulbert A. J. (2003). Docosahexaenoic acid (DHA) content of membranes determines molecular activity of the sodium pump: implications for disease states and metabolism. Naturwissenschaften 90, 521 – 523. doi:10.1007/s00114-003-0470-z
  107. USDA. (2011). USDA National Nutrient Database for Standard Reference. Available at: http://www.ars.usda.gov/Services/docs.htm?docid=8964; see fatty acid composition of corn and pork, cow, and lamb brains
  108. Wasserman G. A., Liu X., Lolacono N. J., Factor-Litvak P., Kline J. K., Popovac D., Morina N., Musabegovic A., Vrenezi N., Capuni-Paracka S., Lekic V., Preteni-Redjepi E., Hadzialjevic S., Slavkovich V., Graziano J. (1997). Lead exposure and intelligence in 7-year-old children: the Yugoslavia Prospective Study. Environ. Health Perspect. 105, 956 – 962. doi:10.1289/ehp.97105956
  109. Whalley L. J., Fox H. C., Wahle K. W., Starr J. M., Deary I. J. (2004). Cognitive aging, childhood intelligence, and the use of food supplements: possible involvement of n-3 fatty acids. Am. J. Clin. Nutr. 80, 1650 – 1657.
  110. Wu A., Ying Z., Gomez-Pinilla F. (2008). Docosahexaenoic acid dietary supplementation enhances the effects of exercise on synaptic plasticity and cognition. Neuroscience 155, 751 – 759. doi:10.1016/j.neuroscience.2008.05.061
  111. Wurtman R. J., Cansev M., Ulus I. H. (2009). Synapse formation is enhanced by oral administration of uridine and DHA, the circulating precursors of brain phosphatides. J. Nutr. Health Aging 13, 189 – 197. doi:10.1007/s12603-009-0056-3
  112. Yoshida S., Yasuda A., Kawazato H., Sakai K., Shimada T., Takeshita M., Yuasa S., Kobayashi T., Watanabe S., Okuyama H. (1997). Synaptic vesicle ultrastructural changes in the rat hippocampus induced by a combination of α-linolenate deficiency and a learning task. J. Neurochem. 68, 1261 – 1268. doi:10.1046/j.1471-4159.1997.68031261.x

Citation

Lassek, W. D. & Gaulin, S. J. C. (2011). Sex Differences in the Relationship of Dietary Fatty Acids to Cognitive Measures in American Children. Frontiers in Evolutionary Neuroscience, Volume 3. https://doi.org/
Received
Accepted
Published
Volume
3 - 2011

Copyright

Copyright © 2011 Lassek and Gaulin.

License: http://www.frontiersin.org/licenseagreement

*Correspondence: William D. Lassek

Article metrics

Views
0
Downloads
0
Citations
0
Shares
0

Related articles

NeuroscienceNeurobiology of human language and its evolution: primate and non-primate perspectivesConstance Scharff, Angela D. Friederici, Michael PetridesNeuroscienceBirdsong: Is It Music to Their Ears?Sarah E. Earp, Donna L. ManeyNeuroscienceLife History Theory and Social PsychologyDonald F. Sacco, Karol Osipowicz