Lutein and Zeaxanthin Influence Brain Function in Older Adults: A Randomized Controlled Trial

Journal of the International Neuropsychological Society

Volumn 24, Issue 1, 2018, Pages 77-90

  Lindbergh, Cutter A ^a   Renzi Hammond, Lisa M ^a   Hammond, Billy R ^a   Terry, Douglas P ^a   Mewborn, Catherine M ^a   Puente, Antonio N ^a   Miller, L Stephen ^a,b  

^a University of Georgia ^*  (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Aging; Carotenoids; Cognition; Diet; Food; Magnetic resonance imaging

Indexed keywords

XANTHOPHYLL; ZEAXANTHIN;

AGED; AGING; CINGULATE GYRUS; COGNITIVE DEFECT; CONTROLLED STUDY; DIAGNOSTIC IMAGING; DIETARY SUPPLEMENT; DRUG EFFECT; FEMALE; HUMAN; INDEPENDENT LIVING; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; RANDOMIZED CONTROLLED TRIAL; VERBAL LEARNING; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; COGNITIVE DYSFUNCTION; DIETARY SUPPLEMENTS; FEMALE; GYRUS CINGULI; HUMANS; INDEPENDENT LIVING; LUTEIN; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PREFRONTAL CORTEX; VERBAL LEARNING; ZEAXANTHINS;

EID: 85023193185     PISSN: 13556177     EISSN: 14697661     Source Type: Journal    
DOI: 10.1017/S1355617717000534     Document Type: Article

References (93)

1. Akbaraly, N.T., Faure, H., Gourlet, V., Favier, A., & Berr, C. (2007). Plasma carotenoid levels and cognitive performance in an elderly population: Results of the EVA Study. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 62(3), 308-316.
2. Akbaraly, T.N., Singh-Manoux, A., Marmot, M.G., & Brunner, E.J. (2009). Education attenuates the association between dietary patterns and cognition. Dementia and Geriatric Cognitive Disorders, 27(2), 147-154.
3. Barbey, A.K., Koenigs, M., & Grafman, J. (2013). Dorsolateral prefrontal contributions to human working memory. Cortex, 49(5), 1195-1205.
4. Beatty, S., Nolan, J., Kavanagh, H., & O'Donovan, O. (2004). Macular pigment optical density and its relationship with serum and dietary levels of lutein and zeaxanthin. Archives of Biochemistry and Biophysics, 430(1), 70-76. http://doi.org/10.1016/j.abb.2004.03.015
5. Bernstein, P.S., Khachik, F., Carvalho, L.S., Muir, G.J., Zhao, D.Y., & Katz, N.B. (2001). Identification and quantitation of carotenoids and their metabolites in the tissues of the human eye. Experimental Eye Research, 72(3), 215-223.
6. Bertram, J.S. (1999). Carotenoids and gene regulation. Nutrition Reviews, 57(6), 182-191. http://doi.org/10.1111/j.1753-4887. 1999.tb06941.x
7. Bitner, B.R., Marcano, D.C., Berlin, J.M., Fabian, R.H., Cherian, L., Culver, J.C., ⋯ Tour, J.M. (2012). Antioxidant carbon particles improve cerebrovascular dysfunction following traumatic brain injury. ACS Nano, 6(9), 8007-8014.
8. Blumenfeld, R.S., Parks, C.M., Yonelinas, A.P., & Ranganath, C. (2011). Putting the pieces together: The role of dorsolateral prefrontal cortex in relational memory encoding. Journal of Cognitive Neuroscience, 23(1), 257-265.
9. Blumenfeld, R.S., & Ranganath, C. (2006). Dorsolateral prefrontal cortex promotes long-term memory formation through its role in working memory organization. The Journal of Neuroscience, 26(3), 916-925.
10. Boespflug, E.L., McNamara, R.K., Eliassen, J.C., Schidler, M.D., & Krikorian, R. (2016). Fish oil supplementation increases eventrelated posterior cingulate activation in older adults with subjective memory impairment. The Journal of Nutrition, Health and Aging, 20(2), 161-169. http://doi.org/10.1007/s12603-015-0609-6
11. Bokov, A., Chaudhuri, A., & Richardson, A. (2004). The role of oxidative damage and stress in aging. Mechanisms of Ageing and Development, 125(10-11), 811-826. http://doi.org/10.1016/j. mad.2004.07.009
12. Bone, R.A., Landrum, J.T., & Tarsis, S.L. (1985). Preliminary identification of the human macular pigment. Vision Research, 25(11), 1531-1535.
13. Bookheimer, S.Y., Renner, B.A., Ekstrom, A., Li, Z., Henning, S.M., Brown, J.A., ⋯ Small, G.W. (2013). Pomegranate juice augments memory and fMRI activity in middle-aged and older adults with mild memory complaints. Evidence-Based Complementary and Alternative Medicine. http://doi.org/10.1155/2013/946298
14. Bookheimer, S.Y., Strojwas, M.H., Cohen, M.S., Saunders, A.M., Pericak-Vance, M.A., Mazziotta, J.C., & Small, G.W. (2000). Patterns of brain activation in people at risk for Alzheimer's disease. The New England Journal of Medicine, 343(7), 450-456. http://doi.org/10.1056/NEJM200008173430701
15. Braskie, M.N., Small, G.W., & Bookheimer, S.Y. (2009). Entorhinal cortex structure and functional MRI response during an associative verbal memory task. Human Brain Mapping, 30(12), 3981-3992. http://doi.org/10.1002/hbm.20823
16. Brickman, A.M., Khan, U.A., Provenzano, F.A., Yeung, L.K., Suzuki, W., Schroeter, H., ⋯ Small, S.A. (2014). Enhancing dentate gyrus function with dietary flavanols improves cognition in older adults. Nature Neuroscience, 17(12), 1798-1803. http://doi.org/10.1038/nn.3850
17. Britton, G., Liaaen-Jensen, S., & Pfander, H. (2004). Carotenoids: Handbook. Basel, Switzerland: Springer.
18. Butterfield, D.A., Bader Lange, M.L., & Sultana, R. (2010). Involvements of the lipid peroxidation product, HNE, in the pathogenesis and progression of Alzheimer's disease. Biochimica et Biophysica Acta, 1801(8), 924-929. http://doi.org/10.1016/j. bbalip.2010.02.005
19. Cabeza, R., & Nyberg, L. (2000). Imaging Cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12(1), 1-47. http://doi.org/10.1162/08989290051137585
20. Clément, F., & Belleville, S. (2009). Test-retest reliability of fMRI verbal episodic memory paradigms in healthy older adults and in persons with mild cognitive impairment. Human Brain Mapping, 30(12), 4033-4047. http://doi.org/10.1002/hbm.20827
21. Craft, N.E., Haitema, T.B., Garnett, K.M., Fitch, K.A., & Dorey, C.K. (2004). Carotenoid, tocopherol, and retinol concentrations in elderly human brain. The Journal of Nutrition, Health and Aging, 8(3), 156-162.
22. D'Esposito, M., Deouell, L.Y., & Gazzaley, A. (2003). Alterations in the BOLD fMRI signal with ageing and disease: A challenge for neuroimaging. Nature Reviews Neuroscience, 4(11), 863-872.
23. Erdman, J.W., Smith, J.W., Kuchan, M.J., Mohn, E.S., Johnson, E.J., Rubakhin, S.S., ⋯ Neuringer, M. (2015). Lutein and brain function. Foods, 4(4), 547-564. http://doi.org/10.3390/foods4040547
24. Faul, F., Erdfelder, E., Buchner, A., & Lang, A.-G. (2009). Statistical power analyses using G∗Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41, 1149-1160.
25. Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G∗Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39, 175-191.
26. Feart, C., Letenneur, L., Helmer, C., Samieri, C., Schalch, W., Etheve, S., ⋯ Barberger-Gateau, P. (2015). Plasma carotenoids are inversely associated with dementia risk in an elderly French cohort. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 71(5), 683-688.
27. Feeney, J., Finucane, C., Savva, G.M., Cronin, H., Beatty, S., Nolan, J.M., & Kenny, R.A. (2013). Low macular pigment optical density is associated with lower cognitive performance in a large, population-based sample of older adults. Neurobiology of Aging, 34(11), 2449-2456. http://doi.org/10.1016/j.neurobiolaging. 2013.05.007
28. Fleck, M.S., Daselaar, S.M., Dobbins, I.G., & Cabeza, R. (2006). Role of prefrontal and anterior cingulate regions in decisionmaking processes shared by memory and nonmemory tasks. Cerebral Cortex, 16(11), 1623-1630.
29. Gasquoine, P.G. (2013). Localization of function in anterior cingulate cortex: From psychosurgery to functional neuroimaging. Neuroscience and Biobehavioral Reviews, 37(3), 340-348.
30. Goekoop, R., Rombouts, S.A., Jonker, C., Hibbel, A., Knol, D.L., Truyen, L., ⋯ Scheltens, P. (2004). Challenging the cholinergic system in mild cognitive impairment: A pharmacological fMRI study. NeuroImage, 23(4), 1450-1459.
31. Hammond, B.R., Johnson, E.J., Russell, R.M., Krinsky, N.I., Yeum, K.J., Edwards, R.B., & Snodderly, D.M. (1997). Dietary modification of human macular pigment density. Investigative Ophthalmology and Visual Science, 38(9), 1795-1801.
32. Hammond, B.R., Wooten, B.R., & Smollon, B. (2005). Assessment of the validity of in vivo methods of measuring human macular pigment optical density. Optometry and Vision Science, 82(5), 387-404.
33. Hassevoort, K.M., Khazoum, S.E., Walker, J.A., Barnett, S.M., Raine, L.B., Hammond, B.R., ⋯ Cohen, N.J. (2017). Macular carotenoids, aerobic fitness, and central adiposity are associated differentially with hippocampal-dependent relational memory in preadolescent children. The Journal of Pediatrics. doi: 10.1016/j. jpeds.2017.01.016
34. Heneka, M.T., Carson, M.J., El Khoury, J., Landreth, G.E., Brosseron, F., Feinstein, D.L., ⋯ Kummer, M.P. (2015). Neuroinflammation in Alzheimer's disease. The Lancet: Neurology, 14(4), 388-405. http://doi.org/10.1016/S1474-4422(15) 70016-5
35. Huang, S., Du, F., Shih, Y.Y.I., Shen, Q., Gonzalez-Lima, F., & Duong, T.Q. (2013). Methylene blue potentiates stimulus-evoked fMRI responses and cerebral oxygen consumption during normoxia and hypoxia. NeuroImage, 72, 237-242.
36. Johnson, E.J. (2012). A possible role for lutein and zeaxanthin in cognitive function in the elderly. The American Journal of Clinical Nutrition, 96(5), 1161-1165.
37. Johnson, E.J. (2014). Role of lutein and zeaxanthin in visual and cognitive function throughout the lifespan. Nutrition Reviews, 72(9), 605-612. http://doi.org/10.1111/nure.12133
38. Johnson, E.J., McDonald, K., Caldarella, S.M., Chung, H., Troen, A. M., & Snodderly, D.M. (2008). Cognitive findings of an exploratory trial of docosahexaenoic acid and lutein supplementation in older women. Nutritional Neuroscience, 11(2), 75-83.
39. Johnson, E.J., Vishwanathan, R., Johnson, M.A., Hausman, D.B., Davey, A., Scott, T.M., ⋯ Poon, L.W. (2013). Relationship between serum and brain carotenoids, α-tocopherol, and retinol concentrations and cognitive performance in the oldest old from the Georgia Centenarian Study. Journal of Aging Research. http://doi.org/10.1155/2013/951786
40. Kang, J.H., Ascherio, A., & Grodstein, F. (2005). Fruit and vegetable consumption and cognitive decline in aging women. Annals of Neurology, 57(5), 713-720. http://doi.org/10.1002/ana.20476
41. Kelly, D., Coen, R.F., Akuffo, K.O., Beatty, S., Dennison, J., Moran, R., ⋯ Nolan, J.M. (2015). Cognitive function and its relationship with macular pigment optical density and serum concentrations of its constituent carotenoids. Journal of Alzheimer's Disease, 48(1), 261-277.
42. Kesse-Guyot, E., Andreeva, V.A., Ducros, V., Jeandel, C., Julia, C., Hercberg, S., & Galan, P. (2014). Carotenoid-rich dietary patterns during midlife and subsequent cognitive function. The British Journal of Nutrition, 111(5), 915-923.
43. Khachik, F., Beecher, G.R., Goli, M.B., & Lusby, W.R. (1991). Separation, identification, and quantification of carotenoids in fruits, vegetables and human plasma by high performance liquid chromatography. Pure and Applied Chemistry, 63(1), 71-80. http://doi.org/10.1351/pac199163010071
44. Krinsky, N.I., Mayne, S.T., & Sies, H. (2004). Carotenoids in Health and Disease. Boca Raton, FL: CRC Press.
45. Kvansakul, J., Rodriguez-Carmona, M., Edgar, D.F., Barker, F.M., Koëpcke, W., Schalch, W., & Barbur, J.L. (2006). Supplementation with the carotenoids lutein or zeaxanthin improves human visual performance. Ophthalmic and Physiological Optics, 26(4), 362-371.
46. Landrum, J.T., Bone, R.A., Joa, H., Kilburn, M.D., Moore, L.L., & Sprague, K.E. (1997). A one year study of the macular pigment: The effect of 140 days of a lutein supplement. Experimental Eye Research, 65(1), 57-62.
47. Lazar, N. (2008). The statistical analysis of functional MRI data. New York, NY: Springer.
48. Lee, Y., Kim, J., & Back, J.H. (2009). The influence of multiple lifestyle behaviors on cognitive function in older persons living in the community. Preventive Medicine, 48(1), 86-90. http://doi.org/10.1016/j.ypmed.2008.10.021
49. Lindbergh, C.A., Mewborn, C., Hammond, B.R., Renzi-Hammond, L.M., Curran-Celentano, J.M., & Miller, L.S. (2016). The relationship of lutein and zeaxanthin levels to neurocognitive functioning: An fMRI study of older adults. Journal of the International Neuropsychological Society, 22, 1-12. doi: 10.1017/S1355617716000850
50. Ma, L., Dou, H.-L., Wu, Y.-Q., Huang, Y.-M., Huang, Y.-B., Xu, X.-R., ⋯ Lin, X.-M. (2012). Lutein and zeaxanthin intake and the risk of age-related macular degeneration: A systematic review and meta-analysis. British Journal of Nutrition, 107(3), 350-359. http://doi.org/10.1017/S0007114511004260
51. Ma, L., Lin, X.M., Zou, Z.Y., Xu, X.R., Li, Y., & Xu, R. (2009). A 12-week lutein supplementation improves visual function in Chinese people with long-term computer display light exposure. British Journal of Nutrition, 102(2), 186-190.
52. MacDonald, A.W., Cohen, J.D., Stenger, V.A., & Carter, C.S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 1835-1838.
53. Maci, S., Fonseca, B., & Zhu, Y. (2016). The role of lutein in brain health and function. Nutrafoods, 15, 179-188. doi: 10.17470/nf-016-1014-3
54. Maldjian, J.A., Laurienti, P.J., & Burdette, J.H. (2004). Precentral gyrus discrepancy in electronic versions of the Talairach Atlas. NeuroImage, 21(1), 450-455.
55. Maldjian, J.A., Laurienti, P.J., Burdette, J.B., & Kraft, R.A. (2003). An automated method for neuroanatomic and cytoarchitectonic atlasbased interrogation of fMRI data sets. NeuroImage, 19, 1233-1239.
56. Malinow, M.R., Feeney-Burns, L., Peterson, L.H., Klein, M.L., & Neuringer, M. (1980). Diet-related macular anomalies in monkeys. Investigative Ophthalmology and Visual Science, 19(8), 857-863.
57. Mares, J.A., LaRowe, T.L., Snodderly, D.M., Moeller, S.M., Gruber, M.J., Klein, M.L., ⋯ Chappell, R.J. (2006). Predictors of optical density of lutein and zeaxanthin in retinas of older women in the Carotenoids in Age-Related Eye Disease Study, an ancillary study of the Women's Health Initiative. The American Journal of Clinical Nutrition, 84(5), 1107-1122.
58. Mazereeuw, G., Lanctôt, K.L., Chau, S.A., Swardfager, W., & Herrmann, N. (2012). Effects of omega-3 fatty acids on cognitive performance: A meta-analysis. Neurobiology of Aging, 33(7), 17-29.
59. Mikkilä, V., Räsänen, L., Raitakari, O.T., Pietinen, P., & Viikari, J. (2005). Consistent dietary patterns identified from childhood to adulthood: The Cardiovascular Risk in Young Finns Study. British Journal of Nutrition, 93(6), 923-931.
60. Min, J., & Min, K. (2014). Serum lycopene, lutein and zeaxanthin, and the risk of Alzheimer's disease mortality in older adults. Dementia and Geriatric Cognitive Disorders, 37(3-4), 246-256.
61. Morris, M.C., Evans, D.A., Tangney, C.C., Bienias, J.L., & Wilson, R.S. (2006). Associations of vegetable and fruit consumption with age-related cognitive change. Neurology, 67(8), 1370-1376. http://doi.org/10.1212/01.wnl.0000240224.38978.d8
62. Murray, I.J., Makridaki, M., van der Veen, R.L., Carden, D., Parry, N.R., & Berendschot, T.T. (2013). Lutein supplementation over a one-year period in early AMD might have a mild beneficial effect on visual acuity: The CLEAR Study. Investigative Ophthalmology & Visual Science, 54(3), 1781-1788.
63. Niendam, T.A., Laird, A.R., Ray, K.L., Dean, Y.M., Glahn, D.C., & Carter, C.S. (2012). Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cognitive, Affective, and Behavioral Neuroscience, 12(2), 241-268.
64. Nolan, J.M., Loskutova, E., Howard, A.N., Moran, R., Mulcahy, R., Stack, J., ⋯ Thurnham, D.I. (2014). Macular pigment, visual function, and macular disease among subjects with Alzheimer's disease: An exploratory study. Journal of Alzheimer's Disease, 42(4), 1191-1202.
65. Nolan, J.M., Stack, J., Mellerio, J., Godhinio, M., O'Donovan, O., Neelam, K., & Beatty, S. (2006). Monthly consistency of macular pigment optical density and serum concentrations of lutein and zeaxanthin. Current Eye Research, 31(2), 199-213.
66. Nyberg, L., Lövdén, M., Riklund, K., Lindenberger, U., & Bäckman, L. (2012). Memory aging and brain maintenance. Trends in Cognitive Sciences, 16(5), 292-305. http://doi.org/10.1016/j.tics.2012.04.005
67. Park, D.C., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173-196. http://doi.org/10.1146/annurev.psych.59.103006.093656
68. Presley, T.D., Morgan, A.R., Bechtold, E., Clodfelter, W., Dove R.W., Jennings, J.M., ⋯ Miller, G.D. (2011). Acute effect of a high nitrate diet on brain perfusion in older adults. Nitric Oxide: Biology and Chemistry, 24(1), 34-42. http://doi.org/10.1016/j. niox.2010.10.002
69. Renzi, L.M., Dengler, M.J., Puente, A., Miller, L.S., & Hammond B.R. (2014). Relationships betweenmacular pigment optical density and cognitive function in unimpaired and mildly cognitively impaired older adults. Neurobiology of Aging, 35(7), 1695-1699. http://doi.org/10.1016/j.neurobiolaging.2013.12.024
70. Renzi, L.M., & Hammond, B.R. (2010). The relation between the macular carotenoids, lutein and zeaxanthin, and temporal vision. Ophthalmic and Physiological Optics, 30(4), 351-357. http://doi.org/10.1111/j.1475-1313.2010.00720.x
71. Renzi, L., Iannaccone, A., Johnson, E., & Kritchevsky, S. (2008). The relation between serum xanthophylls, fatty acids, macular pigment and cognitive function in the Health ABC Study. FASEB Journal, 22, 877.5. doi: 10.1096/fj.1530-6860
72. Reuter-Lorenz, P.A., & Park, D.C. (2014). How does it STAC up? Revisiting the Scaffolding Theory of Aging and Cognition. Neuropsychology Review, 24(3), 355-370. http://doi.org/10.1007/s11065-014-9270-9
73. Rorden, C. (2007). DCM2NII (Computer software).
74. Rosano, C., Marsland, A.L., & Gianaros, P.J. (2012). Maintaining brain health by monitoring inflammatory processes: A mechanism to promote successful aging. Aging and Disease, 3(1), 16-33.
75. Ruitenberg, A., den Heijer, T., Bakker, S.L., van Swieten, J.C., Koudstaal, P.J., Hofman, A., & Breteler, M. (2005). Cerebral hypoperfusion and clinical onset of dementia: The Rotterdam Study. Annals of Neurology, 57(6), 789-794.
76. SanGiovanni, J.P., & Neuringer, M. (2012). The putative role of lutein and zeaxanthin as protective agents against age-related macular degeneration: Promise of molecular genetics for guiding mechanistic and translational research in the field. The American Journal of Clinical Nutrition, 96(5), 1223-1233. doi: http://doi.org/10.3945/ajcn.112.038240
77. Saykin, A.J., Wishart, H.A., Rabin, L.A., Flashman, L.A., McHugh, T.L., Mamourian, A.C., & Santulli, R.B. (2004). Cholinergic enhancement of frontal lobe activity in mild cognitive impairment. Brain, 127(7), 1574-1583.
78. Shenhav, A., Botvinick, M.M., & Cohen, J.D. (2013). The expected value of control: An integrative theory of anterior cingulate cortex function. Neuron, 79(2), 217-240.
79. Stahl, W., & Sies, H. (2001). Effects of carotenoids and retinoids on gap junctional communication. Biofactors, 15(2-4), 95.
80. Stringham, J.M., & Hammond, B.R. (2008). Macular pigment and visual performance under glare conditions. Optometry & Vision Science, 85(2), 82-88.
81. Stringham, J.M., Hammond, B.R., Nolan, J.M., Wooten, B.R., Mammen, A., Smollon, W., & Snodderly, D.M. (2008). The utility of using customized heterochromatic flicker photometry (cHFP) to measure macular pigment in patients with age-related macular degeneration. Experimental Eye Research, 87(5), 445-453.
82. Vishwanathan, R., Iannaccone, A., Scott, T.M., Kritchevsky, S.B., Jennings, B.J., Carboni, G., ⋯ Johnson, E.J. (2014). Macular pigment optical density is related to cognitive function in older people. Age and Ageing, 43(2), 271-275. http://doi.org/10.1093/ageing/aft210
83. Vishwanathan, R., Neuringer, M., Snodderly, D.M., Schalch, W., & Johnson, E.J. (2013). Macular lutein and zeaxanthin are related to brain lutein and zeaxanthin in primates. Nutritional Neuroscience, 16(1), 21-29. http://doi.org/10.1179/147683051 2Y.0000000024
84. Vishwanathan, R., Schalch, W., & Johnson, E.J. (2016). Macular pigment carotenoids in the retina and occipital cortex are related in humans. Nutritional Neuroscience, 19(3), 95-101. http://doi.org/10.1179/1476830514Y.0000000141
85. Wechsler, D. (2001). Wechsler Test of Adult Reading: WTAR. San Antonio, TX: Psychological Corporation.
86. Wechsler, D. (2009). The Wechsler Memory Scale-Fourth Edition (WMS-IV). San Antonio, TX: Pearson Assessments.
87. Weigert, G., Kaya, S., Pemp, B., Sacu, S., Lasta, M., Werkmeister, R.M., ⋯ Schmetterer, L. (2011). Effects of lutein supplementation on macular pigment optical density and visual acuity in patients with age-related macular degeneration. Investigative Ophthalmology & Visual Science, 52(11), 8174-8178.
88. Weissman, D.H., Gopalakrishnan, A., Hazlett, C.J., & Woldorff M.G. (2005). Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. Cerebral Cortex, 15(2), 229-237.
89. Widomska, J., & Subczynski, W.K. (2014). Why has nature chosen lutein and zeaxanthin to protect the retina? Journal of Clinical and Experimental Ophthalmology, 5(1). http://doi.org/10.4172/2155-9570.1000326
90. Wilkinson, D., & Halligan, P. (2004). The relevance of behavioural measures for functional-imaging studies of cognition. Nature Reviews Neuroscience, 5(1), 67-73.
91. Yagi, A., Fujimoto, K., Michihiro, K., Goh, B., Tsi, D., & Nagai, H. (2009). The effect of lutein supplementation on visual fatigue: A psychophysiological analysis. Applied Ergonomics, 40(6), 1047-1054.
92. Yesavage, J.A., Brink, T.L., Rose, T.L., Lum, O., Huang, V., Adey, M., ⋯ Leirer, V.O. (1983). Development and validation of a geriatric depression screening scale: A preliminary report. Journal of Psychiatric Research, 17(1), 37-49. http://doi.org/10.1016/0022-3956(82)90033-4
93. Zamroziewicz, M.K., & Barbey, A.K. (2016). Nutritional cognitive neuroscience: Innovations for healthy brain aging. Frontiers in Neuroscience, 10, 1-10. doi: 10.3389/fnins.2016.00240