1932

Abstract

Appraising success in meeting the world's nutritional needs has largely focused on infant mortality and anthropometric measurements with an emphasis on the first 1,000 days (conception to approximately age 2 years). This ignores the unique nutritional needs of the human brain. Although the intrauterine environment and the early postnatal years are important, equally critical periods follow during which the brain's intricate wiring is established for a lifetime of experience-driven remodeling. At the peak of this process during childhood, the human brain may account for 50% of the body's basal nutritional requirement. Thus, the consequences of proper nutritional management of the brain play out over a lifetime. Our motivation in preparing this review was to move the human brain into a more central position in the planning of nutritional programs. Here we review the macro- and micronutrient requirements of the human brain and how they are delivered, from conception to adulthood.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-082117-051652
2018-08-21
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/nutr/38/1/annurev-nutr-082117-051652.html?itemId=/content/journals/10.1146/annurev-nutr-082117-051652&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Adam PA, Raiha N, Rahiala EL, Kekomaki M 1975. Oxidation of glucose and D-B-OH-butyrate by the early human fetal brain. Acta Paediatr. Scand. 64:17–24
    [Google Scholar]
  2. 2.  Alkire MT, Haier RJ, Barker SJ, Shah NK, Wu JC, Kao YJ 1995. Cerebral metabolism during propofol anesthesia in humans studied with positron emission tomography. Anesthesiology 82:393–403
    [Google Scholar]
  3. 3.  Allen LH 2012. Vitamin B-12. Adv. Nutr. 3:54–55
    [Google Scholar]
  4. 4.  Altman DI, Perlman JM, Volpe JJ, Powers WJ 1993. Cerebral oxygen metabolism in newborns. Pediatrics 92:99–104
    [Google Scholar]
  5. 5.  Andreone BJ, Chow BW, Tata A, Lacoste B, Ben-Zvi A et al. 2017. Blood-brain barrier permeability is regulated by lipid transport-dependent suppression of caveolae-mediated transcytosis. Neuron 94:581–94.e5
    [Google Scholar]
  6. 6.  Astrup J, Sorensen PM, Sorensen HR 1981. Oxygen and glucose consumption related to Na+-K+ transport in canine brain. Stroke 12:726–30
    [Google Scholar]
  7. 7.  Barberger-Gateau P, Letenneur L, Deschamps V, Peres K, Dartigues JF, Renaud S 2002. Fish, meat, and risk of dementia: cohort study. BMJ 325:932–33
    [Google Scholar]
  8. 8.  Barkovich AJ, Ali FA, Rowley HA, Bass N 1998. Imaging patterns of neonatal hypoglycemia. Am. J. Neuroradiol. 19:523–28
    [Google Scholar]
  9. 9.  Barkulis SS, Geiger A, Kawakita Y, Aguilar V 1960. A study on the incorporation of 14C derived from glucose into the free amino acids of the brain cortex. J. Neurochem. 5:339–48
    [Google Scholar]
  10. 10.  Beard JL, Connor JR 2003. Iron status and neural functioning. Annu. Rev. Nutr. 23:41–58
    [Google Scholar]
  11. 11.  Ben-Zvi A, Lacoste B, Kur E, Andreone BJ, Mayshar Y et al. 2014. Mfsd2a is critical for the formation and function of the blood-brain barrier. Nature 509:507–11
    [Google Scholar]
  12. 12.  Black MM, Walker SP, Fernald LCH, Andersen CT, DiGirolamo AM et al. 2017. Early childhood development coming of age: science through the life course. Lancet 389:77–90
    [Google Scholar]
  13. 13.  Blusztajn JK, Mellott TJ 2012. Choline nutrition programs brain development via DNA and histone methylation. Cent. Nerv. Syst. Agents Med. Chem. 12:82–94
    [Google Scholar]
  14. 14.  Boyle PJ, Scott JC, Krentz AJ, Nagy RJ, Comstock E, Hoffman C 1994. Diminished brain glucose metabolism is a significant determinant for falling rates of systemic glucose utilization during sleep in normal humans. J. Clin. Invest. 93:529–35
    [Google Scholar]
  15. 15.  Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A et al. 2014. The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl. Med. 6:263ra158
    [Google Scholar]
  16. 16.  Broadhurst CL, Wang Y, Crawford MA, Cunnane SC, Parkington JE, Schmidt WF 2002. Brain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens. Comp. Biochem. Physiol. B 131:653–73
    [Google Scholar]
  17. 17.  Bruer JT 1999. The Myth of the First Three Years: A New Understanding of Early Brain Development and Lifelong Learning New York: Free Press
  18. 18.  Burns CM, Rutherford MA, Boardman JP, Cowan FM 2008. Patterns of cerebral injury and neurodevelopmental outcomes after symptomatic neonatal hypoglycemia. Pediatrics 122:65–74
    [Google Scholar]
  19. 19.  Caballero B, Allen LH, Prentice A 2013. Encyclopedia of Human Nutrition Amsterdam: Elsevier. , 3rd ed..
  20. 20.  Chugani HT 1987. Positron emission tomography: principles and applications in pediatrics. Mead Johns. Symp. Perinat. Dev. Med. 1987:15–18
    [Google Scholar]
  21. 21.  Chugani HT 1998. A critical period of brain development: studies of cerebral glucose utilization with PET. Prev. Med. 27:184–88
    [Google Scholar]
  22. 22.  Chugani HT, Phelps ME, Mazziotta JC 1987. Positron emission tomography study of human brain functional development. Ann. Neurol. 22:487–97
    [Google Scholar]
  23. 23.  Craig WJ 2009. Health effects of vegan diets. Am. J. Clin. Nutr. 89:1627S–33S
    [Google Scholar]
  24. 24.  Craig WJ, Mangels AR 2009. Position of the American Dietetic Association: vegetarian diets. J. Am. Diet. Assoc. 109:1266–82
    [Google Scholar]
  25. 25.  Cremer JE 1964. Amino acid metabolism in rat brain studied with 14C-labelled glucose. J. Neurochem. 11:165–85
    [Google Scholar]
  26. 26.  Crosby L, Jayasinghe D, McNair D 2013. Food for Thought: Tackling Child Malnutrition to Unlock Potential and Boost Prosperity London: Save Child. Int.
  27. 27.  Cunnane SC, Crawford MA 2014. Energetic and nutritional constraints on infant brain development: implications for brain expansion during human evolution. J. Hum. Evol. 77:88–98
    [Google Scholar]
  28. 28.  Dinan TG, Cryan JF 2017. Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J. Physiol. 595:489–503
    [Google Scholar]
  29. 29.  Eaton JC, Iannotti LL 2017. Genome-nutrition divergence: evolving understanding of the malnutrition spectrum. Nutr. Rev. 75:934–50
    [Google Scholar]
  30. 30.  Engl E, Attwell D 2015. Non-signalling energy use in the brain. J. Physiol. 593:3417–29
    [Google Scholar]
  31. 31.  Fernstrom JD 2013. Large neutral amino acids: dietary effects on brain neurochemistry and function. Amino Acids 45:419–30
    [Google Scholar]
  32. 32.  Fitzpatrick SM, Hetherington HP, Behar KL, Shulman RG 1990. The flux from glucose to glutamate in the rat brain in vivo as determined by 1H-observed, 13C-edited NMR spectroscopy. J. Cereb. Blood Flow Metab. 10:170–79
    [Google Scholar]
  33. 33. Food Agric. Organ. 2017. Nutrition requirements. Food Agric. Organ. United Nations Rome: http://www.fao.org/nutrition/requirements/en/
  34. 34.  Fox PT, Raichle ME 1986. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. PNAS 83:1140–44
    [Google Scholar]
  35. 35.  Fox PT, Raichle ME, Mintun MA, Dence C 1988. Nonoxidative glucose consumption during focal physiologic neural activity. Science 241:462–64
    [Google Scholar]
  36. 36.  Gaitonde MK, Dahl DR, Elliott KA 1965. Entry of glucose carbon into amino acids of rat brain and liver in vivo after injection of uniformly 14C-labelled glucose. Biochem. J. 94:345–52
    [Google Scholar]
  37. 37.  Georgieff MK 2007. Nutrition and the developing brain: nutrient priorities and measurement. Am. J. Clin. Nutr. 85:614S–20S
    [Google Scholar]
  38. 38.  Goyal MS, Hawrylycz M, Miller JA, Snyder AZ, Raichle ME 2014. Aerobic glycolysis in the human brain is associated with development and neotenous gene expression. Cell Metab 19:49–57
    [Google Scholar]
  39. 39.  Goyal MS, Raichle ME 2013. Gene expression-based modeling of human cortical synaptic density. PNAS 110:6571–76
    [Google Scholar]
  40. 40.  Goyal MS, Venkatesh S, Milbrandt J, Gordon JI, Raichle ME 2015. Feeding the brain and nurturing the mind: linking nutrition and the gut microbiota to brain development. PNAS 112:14105–12
    [Google Scholar]
  41. 41.  Goyal MS, Vlassenko AG, Blazey TM, Su Y, Couture LE et al. 2017. Loss of brain aerobic glycolysis in normal human aging. Cell Metab 26:353–60.e3
    [Google Scholar]
  42. 42.  Green R, Allen LH, Bjørke-Monsen AL, Brito A, Gueant JL et al. 2017. Vitamin B12 deficiency. Nat. Rev. Dis. Primers 3:17040
    [Google Scholar]
  43. 43.  Gruetter R, Novotny EJ, Boulware SD, Mason GF, Rothman DL et al. 1994. Localized 13C NMR spectroscopy in the human brain of amino acid labeling from d-[1-13C]glucose. J. Neurochem. 63:1377–85
    [Google Scholar]
  44. 44.  Hadley KB, Ryan AS, Forsyth S, Gautier S, Salem N Jr 2016. The essentiality of arachidonic acid in infant development. Nutrients 8:216
    [Google Scholar]
  45. 45.  Holtmaat A, Svoboda K 2009. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 10:647–58
    [Google Scholar]
  46. 46.  Hui S, Ghergurovich JM, Morscher RJ, Jang C, Teng X et al. 2017. Glucose feeds the TCA cycle via circulating lactate. Nature 551:115–18
    [Google Scholar]
  47. 47.  Huttenlocher PR, Dabholkar AS 1997. Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387:167–78
    [Google Scholar]
  48. 48.  Iannotti LL, Lutter CK, Waters WF, Gallegos Riofrio CA, Malo C et al. 2017. Eggs early in complementary feeding increase choline pathway biomarkers and DHA: a randomized controlled trial in Ecuador. Am. J. Clin. Nutr. 106:1482–89
    [Google Scholar]
  49. 49.  Ide K, Secher NH 2000. Cerebral blood flow and metabolism during exercise. Prog. Neurobiol. 61:397–414
    [Google Scholar]
  50. 50.  Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X et al. 2011. Spatio-temporal transcriptome of the human brain. Nature 478:483–89
    [Google Scholar]
  51. 51.  Kennedy C, Sokoloff L 1957. An adaptation of the nitrous oxide method to the study of the cerebral circulation in children: normal values for cerebral blood flow and cerebral metabolic rate in childhood. J. Clin. Invest. 36:1130–37
    [Google Scholar]
  52. 52.  Kennedy DO 2016. B vitamins and the brain: mechanisms, dose and efficacy—a review. Nutrients 8:68
    [Google Scholar]
  53. 53.  Kety SS 1950. Circulation and metabolism of the human brain in health and disease. Am. J. Med. 8:205–17
    [Google Scholar]
  54. 54.  Kety SS, Schmidt CF 1948. The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values. J. Clin. Invest. 27:476–83
    [Google Scholar]
  55. 55.  Kinnala A, Suhonen-Polvi H, Aarimaa T, Kero P, Korvenranta H et al. 1996. Cerebral metabolic rate for glucose during the first six months of life: an FDG positron emission tomography study. Arch. Dis. Child Fetal Neonatal Ed. 74:F153–57
    [Google Scholar]
  56. 56.  Kretchmer N, Beard JL, Carlson S 1996. The role of nutrition in the development of normal cognition. Am. J. Clin. Nutr. 63:997S–1001S
    [Google Scholar]
  57. 57.  Kuzawa CW, Chugani HT, Grossman LI, Lipovich L, Muzik O et al. 2014. Metabolic costs and evolutionary implications of human brain development. PNAS 111:13010–15
    [Google Scholar]
  58. 58.  Kwik-Uribe CL, Gietzen D, German JB, Golub MS, Keen CL 2000. Chronic marginal iron intakes during early development in mice result in persistent changes in dopamine metabolism and myelin composition. J. Nutr. 130:2821–30
    [Google Scholar]
  59. 59.  Levenson CW, Morris D 2011. Zinc and neurogenesis: making new neurons from development to adulthood. Adv. Nutr. 2:96–100
    [Google Scholar]
  60. 60.  Liberti MV, Locasale JW 2016. The Warburg effect: How does it benefit cancer cells?. Trends Biochem. Sci. 41:211–18
    [Google Scholar]
  61. 61.  Lopes-Cardozo M, Larsson OM, Schousboe A 1986. Acetoacetate and glucose as lipid precursors and energy substrates in primary cultures of astrocytes and neurons from mouse cerebral cortex. J. Neurochem. 46:773–78
    [Google Scholar]
  62. 62.  Lozoff B 2011. Early iron deficiency has brain and behavior effects consistent with dopaminergic dysfunction. J. Nutr. 141:740S–46S
    [Google Scholar]
  63. 63.  Lunt SY, Vander Heiden MG 2011. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu. Rev. Cell Dev. Biol. 27:441–64
    [Google Scholar]
  64. 64.  Mann J, Truswell AS, eds. 2012. Essentials of Human Nutrition Oxford, UK: Oxford Univ. Press. , 2nd ed..
  65. 65.  Marder E, Goaillard JM 2006. Variability, compensation and homeostasis in neuron and network function. Nat. Rev. Neurosci. 7:563–74
    [Google Scholar]
  66. 66.  Marger L, Schubert CR, Bertrand D 2014. Zinc: an underappreciated modulatory factor of brain function. Biochem. Pharmacol. 91:426–35
    [Google Scholar]
  67. 67.  Matsumoto M, Kibe R, Ooga T, Aiba Y, Sawaki E et al. 2013. Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study. Front. Syst. Neurosci. 7:9
    [Google Scholar]
  68. 68.  Mehta S, Kalsi HK, Nain CK, Menkes JH 1977. Energy metabolism of brain in human protein-calorie malnutrition. Pediatr. Res. 11:290–93
    [Google Scholar]
  69. 69.  Mink JW, Blumenschine RJ, Adams DB 1981. Ratio of central nervous system to body metabolism in vertebrates: its constancy and functional basis. Am. J. Physiol. 241:R203–12
    [Google Scholar]
  70. 70.  Moos T, Rosengren Nielsen T, Skjorringe T, Morgan EH 2007. Iron trafficking inside the brain. J. Neurochem. 103:1730–40
    [Google Scholar]
  71. 71.  Morris MC, Evans DA, Bienias JL, Tangney CC, Bennett DA et al. 2003. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch. Neurol. 60:940–46
    [Google Scholar]
  72. 72.  Nguyen LN, Ma D, Shui G, Wong P, Cazenave-Gassiot A et al. 2014. Mfsd2a is a transporter for the essential omega-3 fatty acid docosahexaenoic acid. Nature 509:503–6
    [Google Scholar]
  73. 73.  Oken E, Kleinman KP, Berland WE, Simon SR, Rich-Edwards JW, Gillman MW 2003. Decline in fish consumption among pregnant women after a national mercury advisory. Obstet. Gynecol. 102:346–51
    [Google Scholar]
  74. 74.  Penland JG, Prohaska JR 2004. Abnormal motor function persists following recovery from perinatal copper deficiency in rats. J. Nutr. 134:1984–88
    [Google Scholar]
  75. 75.  Prado EL, Dewey KG 2014. Nutrition and brain development in early life. Nutr. Rev. 72:267–84
    [Google Scholar]
  76. 76.  Rao R, Tkac I, Schmidt AT, Georgieff MK 2011. Fetal and neonatal iron deficiency causes volume loss and alters the neurochemical profile of the adult rat hippocampus. Nutr. Neurosci. 14:59–65
    [Google Scholar]
  77. 77.  Redman K, Ruffman T, Fitzgerald P, Skeaff S 2016. Iodine deficiency and the brain: effects and mechanisms. Crit. Rev. Food Sci. Nutr. 56:2695–713
    [Google Scholar]
  78. 78.  Ripps H, Shen W 2012. Taurine: a “very essential” amino acid. Mol. Vis. 18:2673–86
    [Google Scholar]
  79. 79.  Saari JC 2016. Vitamin A and vision. Sub-Cell. Biochem. 81:231–59
    [Google Scholar]
  80. 80.  Sandstead HH 2012. Subclinical zinc deficiency impairs human brain function. J. Trace Elem. Med. Biol. 26:70–73
    [Google Scholar]
  81. 81. Save Child. Int. 2012. State of the World's Mothers 2012: Nutrition in the First 1,000 Days London: Save Child. Int.
  82. 82.  Scheiber IF, Dringen R 2013. Astrocyte functions in the copper homeostasis of the brain. Neurochem. Int. 62:556–65
    [Google Scholar]
  83. 83.  Segarra‐Mondejar M, Casellas‐Díaz S, Ramiro‐Pareta M, Müller‐Sánchez C, Martorell‐Riera A et al. 2018. Synaptic activity–induced glycolysis facilitates membrane lipid provision and neurite outgrowth. EMBO J 37:e97368
    [Google Scholar]
  84. 84.  Shah SN, Peterson NA, McKean CM 1970. Cerebral lipid metabolism in experimental hyperphenylalaninaemia: incorporation of 14C-labelled glucose into total lipids. J. Neurochem. 17:279–84
    [Google Scholar]
  85. 85.  Shan ZY, Leiker AJ, Onar-Thomas A, Li Y, Feng T et al. 2014. Cerebral glucose metabolism on positron emission tomography of children. Hum. Brain Mapp. 35:2297–309
    [Google Scholar]
  86. 86.  Shannon BJ, Vaishnavi SN, Vlassenko AG, Shimony JS, Rutlin J, Raichle ME 2016. Brain aerobic glycolysis and motor adaptation learning. PNAS 113:E3782–91
    [Google Scholar]
  87. 87.  Shearer KD, Stoney PN, Morgan PJ, McCaffery PJ 2012. A vitamin for the brain. Trends Neurosci 35:733–41
    [Google Scholar]
  88. 88.  Spector R, Johanson CE 2014. The nexus of vitamin homeostasis and DNA synthesis and modification in mammalian brain. Mol. Brain 7:3
    [Google Scholar]
  89. 89.  Starling P, Charlton K, McMahon AT, Lucas C 2015. Fish intake during pregnancy and foetal neurodevelopment—a systematic review of the evidence. Nutrients 7:2001–14
    [Google Scholar]
  90. 90.  Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M et al. 2014. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510:417–21
    [Google Scholar]
  91. 91.  Torres-Vega A, Pliego-Rivero BF, Otero-Ojeda GA, Gomez-Olivan LM, Vieyra-Reyes P 2012. Limbic system pathologies associated with deficiencies and excesses of the trace elements iron, zinc, copper, and selenium. Nutr. Rev. 70:679–92
    [Google Scholar]
  92. 92.  Uauy R, Dangour AD 2006. Nutrition in brain development and aging: role of essential fatty acids. Nutr. Rev. 64:S24–33
    [Google Scholar]
  93. 93.  Uchida Y, Ito K, Ohtsuki S, Kubo Y, Suzuki T, Terasaki T 2015. Major involvement of Na+-dependent multivitamin transporter (SLC5A6/SMVT) in uptake of biotin and pantothenic acid by human brain capillary endothelial cells. J. Neurochem. 134:97–112
    [Google Scholar]
  94. 94. US Environ. Prot. Agency. 2017. 2017 EPA-FDA advice about eating fish and shellfish. US Environ. Prot. Agency Washington, DC: https://www.epa.gov/fish-tech/2017-epa-fda-advice-about-eating-fish-and-shellfish
  95. 95.  Vaishnavi SN, Vlassenko AG, Rundle MM, Snyder AZ, Mintun MA, Raichle ME 2010. Regional aerobic glycolysis in the human brain. PNAS 107:17757–62
    [Google Scholar]
  96. 96.  Vrba R, Gaitonde MK, Richter D 1962. The conversion of glucose carbon into protein in the brain and other organs of the rat. J. Neurochem. 9:465–75
    [Google Scholar]
  97. 97.  Vuong HE, Yano JM, Fung TC, Hsiao EY 2017. The microbiome and host behavior. Annu. Rev. Neurosci. 40:21–49
    [Google Scholar]
  98. 98.  Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L 2014. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol 13:1045–60
    [Google Scholar]
  99. 99.  Weiser MJ, Butt CM, Mohajeri MH 2016. Docosahexaenoic acid and cognition throughout the lifespan. Nutrients 8:99
    [Google Scholar]
  100. 100.  Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA et al. 2009. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. PNAS 106:3698–703
    [Google Scholar]
  101. 101.  World Health Organ 2017. Dietary recommendations/nutritional requirements. World Health Organ., Geneva. http://www.who.int/nutrition/topics/nutrecomm/en/
  102. 100a. World Health Organ. 2001. Iron Deficiency Anaemia: Assessment, Prevention and Control Geneva, World Health Organ.
  103. 102.  World Health Organ 2017. Micronutrient deficiencies: iodine deficiency disorders.. World Health Organ., Geneva. http://www.who.int/nutrition/topics/idd/en/
  104. 103.  Yao LP, Bandres J, Nemoto EM, Boston JR, Darby JM, Yonas H 1992. Effect of 33% xenon inhalation on whole-brain blood flow and metabolism in awake and fentanyl-anesthetized monkeys. Stroke 23:69–74
    [Google Scholar]
  105. 104.  Yoxall CW, Weindling AM 1998. Measurement of cerebral oxygen consumption in the human neonate using near infrared spectroscopy: Cerebral oxygen consumption increases with advancing gestational age. Pediatr. Res. 44:283–90
    [Google Scholar]
  106. 105.  Zeisel SH 2006. The fetal origins of memory: the role of dietary choline in optimal brain development. J. Pediatr. 149:S131–36
    [Google Scholar]
/content/journals/10.1146/annurev-nutr-082117-051652
Loading
/content/journals/10.1146/annurev-nutr-082117-051652
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error