Relationship of Lutein and Zeaxanthin Levels to Neurocognitive Functioning: An fMRI Study of Older Adults

Journal of the International Neuropsychological Society

Volumn 23, Issue 1, 2017, Pages 11-22

  Lindbergh, Cutter A ^a   Mewborn, Catherine M ^a   Hammond, Billy R ^a   Renzi Hammond, Lisa M ^a   Curran Celentano, Joanne M ^b   Miller, L Stephen ^a,c  

^a University of Georgia   (United States)

^b UNIVERSITY OF NEW HAMPSHIRE   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

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

Indexed keywords

OXYGEN; VISUAL PIGMENT; XANTHOPHYLL; ZEAXANTHIN;

AGED; AGING; BLOOD; BRAIN; BRAIN MAPPING; COGNITIVE AGING; DEPRESSION; DIAGNOSTIC IMAGING; FEMALE; HUMAN; IMAGE PROCESSING; INDEPENDENT LIVING; MALE; METABOLISM; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; READING; VERBAL LEARNING; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; BRAIN; BRAIN MAPPING; COGNITIVE AGING; DEPRESSION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDEPENDENT LIVING; LUTEIN; MACULAR PIGMENT; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; OXYGEN; READING; VERBAL LEARNING; ZEAXANTHINS;

EID: 84992406263     PISSN: 13556177     EISSN: 14697661     Source Type: Journal    
DOI: 10.1017/S1355617716000850     Document Type: Article

References (85)

1. Akbaraly, N., Faure, H., Gourlet, V., Favier, A., Berr, C. (2007).Plasma carotenoid levels and cognitive performance in an elderlypopulation: Results of the EVA study. Journals of Gerontology, Series A, Biological Sciences and Medical Sciences, 62(3), 308-316.
2. Arnal, E., Miranda, M., Barcia, J., Bosch-Morell, F., Romero, F.(2010). Lutein and docosahexaenoic acid prevent cortex lipidperoxidation in streptozotocin-induced diabetic rat cerebralcortex. Journal of Neuroscience, 166(1), 271-278.
3. Baker, C., Peli, E., Knouf, N., Kanwisher, N. (2005).Reorganization of visual processing in macular degeneration.Journal of Neuroscience, 25(3), 614-618.
4. Banich, M. (1998). The missing link: The role of interhemisphericinteraction in attentional processing. Brain and Cognition, 36(2), 128-157.
5. Beatty, S., Nolan, J., Kavanagh, H., O'Donovan, O. (2004).Macular pigment optical density and its relationship with serumand dietary levels of lutein and zeaxanthin. Archives ofBiochemistry and Biophysics, 430, 70-76.
6. Bian, Q., Gao, S., Zhou, J., Qin, J., Taylor, A., Johnson, E., ...Shang, F. (2012). Lutein and zeaxanthin supplementation reducesphotooxidative damage and modulates the expression ofinflammation-related genes in retinal pigment epithelial cells.Free Radical Biology and Medicine, 53(6), 1298-1307.
7. Binawade, Y., Jagtap, A. (2013). Neuroprotective effect of luteinagainst 3-nitropropionic acid-induced Huntington's disease-likesymptoms: Possible behavioral, biochemical, cellular alterations.Journal of Medicinal Food, 16(10), 934-943.
8. Binder, J.R., Desai, R.H., Graves, W.W., Conant, L.L. (2009).Where is the semantic system A critical review and metaanalysisof 120 functional neuroimaging studies. CerebralCortex, 19(12), 2767-2796.
9. Bookheimer, S., Renner, B., Ekstrom, A., Li, Z., Henning, S., Brown, J., Small, G. (2013). Pomegranate juice augmentsmemory and fMRI activity in middle-aged and older adults withmild memory complaints. Evidence-Based Complementary andAlternative Medicine, 2013, 946298.
10. Bookheimer, S., Strojwas, M., Cohen, M., Saunders, A., Pericak-Vance, M., Mazziotta, J., Small, G. (2000). Patterns of brainactivation in people at risk for Alzheimer's disease. New EnglandJournal of Medicine, 343(7), 450-456.
11. Bone, R.A., Landrum, J.T., Dixon, Z., Chen, Y., Llerena, C.M.(2000). Lutein and zeaxanthin in the eyes, serum and diet ofhuman subjects. Experimental Eye Research, 71(3), 239-245.
12. Bone, R., Landrum, J., Tarsis, S. (1985). Preliminary identificationof the human macular pigment. Vision Research, 25(11), 1531-1535.
13. Braskie, M., Small, G., Bookheimer, S. (2009). Entorhinal cortexstructure and functional MRI response during an associativeverbal memory task. Human Brain Mapping, 30(12), 3981-3992.
14. Burke, J., Curran-Celentano, J., Wenzel, A. (2005). Diet andserum carotenoid concentrations affect macular pigment opticaldensity in adults 45 years and older. Journal of Nutrition, 135(5), 1208-1214.
15. Cabeza, R., Anderson, N., Locantore, J., McIntosh, A. (2002).Aging gracefully: Compensatory brain activity in highperformingolder adults. Neuroimage, 17(3), 1394-1402.
16. Cabeza, R., Grady, C., Nyberg, L., McIntosh, A., Tulving, E., Kapur, S., Craik, F. (1997). Age-related differences in neuralactivity during memory encoding and retrieval: A positronemission tomography study. Journal of Neuroscience, 17(1), 391-400.
17. Cabeza, R., Nyberg, L. (2000). Imaging Cognition II: Anempirical review of 275 PET and fMRI studies. Journal ofCognitive Neuroscience, 12(1), 1-47.
18. Cardinault, N., Gorrand, J., Tyssandier, V., Grolier, P., Rock, E., Borel, P. (2003). Short-term supplementation with lutein affectsbiomarkers of lutein status similarly in young and elderlysubjects. Experimental Gerontology, 38, 573-582.
19. Clément, F., Belleville, S. (2009). Test-retest reliability of fMRIverbal episodic memory paradigms in healthy older adults and inpersons with mild cognitive impairment. Human Brain Mapping, 30(12), 4033-4047.
20. Chew, E., Clemons, T., SanGiovanni, J., Danis, R., Ferris, F., Elman, M., ...Fish, G. (2014). Secondary analyses of the effectsof lutein/zeaxanthin on age-related macular degenerationprogression: AREDS2 Report No. 3. Journal of the AmericanMedical Association Ophthalmology, 132(2), 142-149.
21. Chew, E., Clemons, T., Agrón, E., Launer, L., Grodstein, F., Bernstein, P. (2015). Effect of omega-3 fatty acids, lutein/zeaxanthin, or other nutrient supplementation on cognitivefunction: The AREDS2 randomized clinical trial. Journal of theAmerican Medical Association, 314(8), 791-801.
22. Convit, A., de Asis, J., de Leon, M., Tarshish, C., De Santi, S., Rusinek, H. (2000). Atrophy of the medial occipitotemporal, inferior, middle temporal gyri in non-demented elderlypredict decline to Alzheimer's disease. Neurobiology of Aging, 21(1), 19-26.
23. Costafreda, S., Fu, C., Lee, L., Everitt, B., Brammer, M., David, A. (2006). A systematic review and quantitative appraisal offMRI studies of verbal fluency: Role of the left inferiorfrontal gyrus. Human Brain Mapping, 27(10), 799-810.
24. Craft, N., Haitema, T., Garnett, K., Fitch, K., Dorey, C. (2004).Carotenoid, tocopherol, retinol concentrations in elderlyhuman brain. Journal of Nutrition Health and Aging, 8(3), 156-162.
25. Dickerson, B., Salat, D., Bates, J., Atiya, M., Killiany, R., Greve, D., Sperling, R.A. (2004). Medial temporal lobefunction and structure in mild cognitive impairment. Annals ofNeurology, 56(1), 27-35.
26. Dickerson, B., Sperling, R. (2008). Functional abnormalities ofthe medial temporal lobe memory system in mild cognitiveimpairment and Alzheimer's disease: Insights from functionalMRI studies. Neuropsychologia, 46(6), 1624-1635.
27. Eickhoff, S., Jbabdi, S., Caspers, S., Laird, A., Fox, P., Zilles, K., Behrens, T. (2010). Anatomical and functional connectivity ofcytoarchitectonic areas within the human parietal operculum.Journal of Neuroscience, 30(18), 6409-6421.
28. Engelhart, M.J., Geerlings, M.I., Meijer, J., Kiliaan, A., Ruitenberg, A., van Swieten, J.C., Breteler, M.M. (2004). Inflammatoryproteins in plasma and the risk of dementia: The RotterdamStudy. Archives of Neurology, 61(5), 668-672.
29. Feart, C., Letenneur, L., Helmer, C., Samieri, C., Schalch, W., Etheve, S., Barberger-Gateau, P. (2016). Plasma carotenoidsare inversely associated with dementia risk in an elderlyFrench cohort. Journals of Gerontology, Series A, BiologicalSciences and Medical Sciences, 71(5), 683-688.
30. Feeney, J., Finucane, C., Savva, G.M., Cronin, H., Beatty, S., Nolan, J.M., Kenny, R.A. (2013). Low macular pigmentoptical density is associated with lower cognitive performance ina large, population-based sample of older adults. Neurobiology ofAging, 34(11), 2449-2456.
31. Fera, F., Weickert, T.W., Goldberg, T.E., Tessitore, A., Hariri, A., Das, S., Mattay, V. (2005). Neural mechanisms underlyingprobabilistic category learning in normal aging. Journal ofNeuroscience, 25(49), 11340-11348.
32. Finkel, T., Holbrook, N. (2000). Oxidants, oxidative stress andthe biology of ageing. Nature, 408(6809), 239-247.
33. Friederici, A., Meyer, M., von Cramon, D. (2000). Auditorylanguage comprehension: An event-related fMRI study on theprocessing of syntactic and lexical information. Brain andLanguage, 74(2), 289-300.
34. Gutchess, A., Welsh, R., Hedden, T., Bangert, A., Minear, M., Liu, L., Park, D. (2005). Aging and the neural correlates ofsuccessful picture encoding: Frontal activations compensatefor decreased medial-temporal activity. Journal of CognitiveNeuroscience, 17(1), 84-96.
35. Hammond, B.R., Johnson, E.J., Russell, R.M., Krinsky, N., Yeum, K., Edwards, R., Snodderly, D. (1997). Dietarymodification of human macular pigment density. InvestigativeOpthalmology, Visual Science, 38(9), 1795-1801.
36. Hammond, B., Wooten, B., Smollon, B. (2005). Assessment ofthe validity of in vivo methods of measuring human macularpigment optical density. Optometry, Vision Science, 82(5), 387-404.
37. Handelman, G.J., Shen, B., Krinksy, N.I. (1992). High resolutionanalysis of carotenoids in human plasma by high-performanceliquid chromatography. Methods in Enzymology, 213, 336-346.
38. Hillary, F.G., Genova, H.M., Chiaravalloti, N.D., Rypma, B., DeLuca, J. (2006). Prefrontal modulation of working memoryperformance in brain injury and disease. Human Brain Mapping, 27(11), 837-847.
39. Huang, C.-M., Polk, T., Goh, J., Park, D. (2012). Both left andright posterior parietal activations contribute to compensatoryprocesses in normal aging. Neuropsychologia, 50(1), 55-66.
40. Johnson, E.J. (2012). A possible role for lutein and zeaxanthin incognitive function in the elderly. American Journal of ClinicalNutrition, 96(5), 1161-1165.
41. Johnson, E. (2014). Role of lutein and zeaxanthin in visual andcognitive function throughout the lifespan. Nutrition Reviews, 72(9), 605-612.
42. Johnson, E., Maras, J.E., Rasmussen, H.M., Tucker, K.L. (2010).Intake of lutein and zeaxanthin differ with age, sex, ethnicity.Journal of the American Dietetic Association, 110(9), 1357-1362.
43. Johnson, E., McDonald, K., Caldarella, S., Chung, H., Troen, A., Snodderly, D. (2008). Cognitive findings of an exploratory trial ofdocosahexaenoic acid and lutein supplementation inolder women. Nutritional Neuroscience, 11(2), 75-83.
44. Johnson, E.J., Vishwanathan, R., Johnson, M.A., Hausman, D.B., Davey, A., Scott, T.M., Poon, L.W. (2013). Relationshipbetween serum and brain carotenoids,-tocopherol, retinolconcentrations and cognitive performance in the oldest old fromthe Georgia Centenarian Study. Journal of Aging Research, 2013, 951786.
45. Kang, J., Ascherio, A., Grodstein, F. (2005). Fruit and vegetableconsumption and cognitive decline in aging women. Annals ofNeurology, 57(5), 713-720.
46. Krinsky, N. (2002). Possible biologic mechanisms for a protectiverole of xanthophylls. The Journal of Nutrition, 132(3), 540-542.
47. Krinsky, N., Mayne, S., Sies, H. (2004). Carotenoids in healthand disease. Florida: CRC Press.
48. Kuhad, A., Sethi, R., Chopra, K. (2008). Lycopene attenuatesdiabetes-associated cognitive decline in rats. Life Sciences, 83(3-4), 128-134.
49. Lazar, N. (2008). The statistical analysis of functional MRI data.New York: Springer.
50. Li, S., Fung, F., Fu, Z., Wong, D., Chan, H., Lo, A. (2012). Antiinflammatoryeffects of lutein in retinal ischemic/hypoxic injury:In vivo and in vitro studies. Investigative Ophthalmology andVisual Science, 53(10), 5976-5984.
51. Lorenzi, M.M., Beltramello, A., Mercuri, N.B., Canu, E., Zoccatelli, G., Pizzini, F.B., ...Frisoni, G.B. (2011). Effect of memantine on restingstate default mode network activity in Alzheimer's disease. Drugsand Aging, 28(3), 205-217.
52. Min, J., Min, K. (2014). Serum lycopene, lutein and zeaxanthin, the risk of Alzheimer's disease mortality in olderadults. Dementia and Geriatric Cognitive Disorders, 37(3-4), 246-256.
53. Molholm, S., Sehatpour, P., Mehta, A.D., Shpaner, M., Gomez-Ramirez, M., Ortigue, S., Foxe, J.J. (2006). Audio-visualmultisensory integration in superior parietal lobule revealed byhuman intracranial recordings. Journal of Neurophysiology, 96(2), 721-729.
54. Morris, M.C., Evans, D., Tangney, C., Bienias, J., Wilson, R.S.(2006). Associations of vegetable and fruit consumption withage-related cognitive change. Neurology, 67(8), 1370-1376.
55. Muriach, M., Bosch-Morell, F., Alexander, G., Blomhoff, R., Barcia, J., Arnal, E., Miranda, M. (2006). Lutein effect onretina and hippocampus of diabetic mice. Free Radical Biologyand Medicine, 41(6), 979-984.
56. Nakashima, Y., Ohsawa, I., Konishi, F., Hasegawa, T., Kumamoto, S., Suzuki, Y., Ohta, S. (2009). Preventive effectsof Chlorella on cognitive decline in age-dependent dementiamodel mice. Neuroscience Letters, 464(3), 193-198.
57. Nolan, J.M., Loskutova, E., Howard, A.N., Moran, R., Mulcahy, R., Stack, J., ...Beatty, S. (2014). Macular pigment, visual function, macular disease among subjects with Alzheimer's disease:An exploratory study. Journal of Alzheimer's Disease, 42(4), 1191-1202.
58. Nolan, J.M., Stack, J., Mellerio, J., Godhinio, M., O'Donovan, O., Neelam, K., Beatty, S. (2006). Monthly consistency of macularpigment optical density and serum concentrations of lutein andzeaxanthin. Current Eye Research, 31(2), 199-213.
59. Olmedilla-Alonso, B., Beltrán-de-Miguel, B., Estévez-Santiago, R., Cuadrado-Vives, C. (2014). Markers of lutein and zeaxanthinstatus in two age groups of men and women: Dietary intake, serum concentrations, lipid profile and macular pigment opticaldensity. Nutrition Journal, 13(1), 142-160.
60. Pappolla, M.A., Smith, M.A., Bryant-Thomas, T., Bazan, N., Petanceska, S., Perry, G., Refolo, L.M. (2002). Cholesterol, oxidative stress, Alzheimer's disease: Expanding thehorizons of pathogenesis. Free Radical Biology and Medicine, 33(2), 173-181.
61. Park, D.C., Reuter-Lorenz, P. (2009). The adaptive brain: Agingand neurocognitive scaffolding. Annual Review of Psychology, 60, 173-196.
62. Petersen, S.E., Van Mier, H., Fiez, J.A., Raichle, M.E. (1998).The effects of practice on the functional anatomy of taskperformance. Proceedings of the National Academy of Sciencesof the United States of America, 95(3), 853-860.
63. Qin, J.Y., Yeum, K.J., Johnson, E.J., Krinsky, N.I., Russell, R.M., Tang, G. (2008). Determination of 9-cis-carotene and-carotene in biological samples. Journal of Nutritional Biochemistry, 19(9), 612-618.
64. Rajah, M.N., Languay, R., Grady, C.L. (2011). Age-relatedchanges in right middle frontal gyrus volume correlate withaltered episodic retrieval activity. Journal of Neuroscience, 31(49), 17941-17954.
65. Renzi, L., Hammond, B.R. (2010). The relation between themacular carotenoids, lutein and zeaxanthin, temporal vision.Ophthalmic and Physiological Optics, 30(4), 351-357.
66. Renzi, L.M., Hammond, B.R., Dengler, M., Roberts, R. (2012).The relation between serum lipids and lutein and zeaxanthin in theserum and retina: Results from cross-sectional, case-control andcase study designs. Lipids in Health and Disease, 11(1), 1-10.
67. Renzi, L.M., Dengler, M.J., Puente, A., Miller, L.S., Hammond, B.R., Jr. (2014). Relationships betweenmacular pigment optical density andcognitive function in unimpaired and mildly cognitively impairedolder adults. Neurobiology of Aging, 35(7), 1695-1699.
68. Rinaldi, P., Polidori, M., Metastasio, A., Mariani, E., Mattioli, P., Cherubini, A., Mecocci, P. (2003). Plasma antioxidants aresimilarly depleted in mild cognitive impairment and inAlzheimer's disease. Neurobiology of Aging, 24(7), 915-919.
69. Rorden, C. (2007). DCM2NII (Computer software). Retrieved fromhttps://www.nitrc.org/projects/dcm2nii/
70. Sasaki, M., Ozawa, Y., Kurihara, T., Noda, K., Imamura, Y., Kobayashi, S., Tsubota, K. (2009). Neuroprotective effect ofan antioxidant, lutein, during retinal inflammation. InvestigativeOpthalmology and Visual Science, 50(3), 1433.
71. Saykin, A.J., Flashman, L.A., Frutiger, S.A., Johnson, S.C., Mamourian, A.C., Moritz, C.H., Weaver, J.B. (1999).Neuroanatomic substrates of semantic memory impairment inAlzheimer's disease: Patterns of functional MRI activation.Journal of the International Neuropsychological Society, 5(5), 377-392.
72. Scanlon, G., Connell, P., Ratzlaff, M., Foerg, B., McCartney, D., Murphy, A., Loughman, J. (2015). Macular pigment opticaldensity is lower in type 2 diabetes, compared with type 1 diabetesand normal controls. Retina, 35(9), 1808-1816.
73. Stahl, W., Sies, H. (2001). Effects of carotenoids and retinoids ongap junctional communication. Biofactors, 15(24), 95-98.
74. Stringham, J.M., Hammond, B.R., Nolan, J.M., Wooten, B.R., Mammen, A., Smollon, W., Snodderly, D.M. (2008). The utilityof using customized heterochromatic flicker photometry (cHFP) tomeasure macular pigment in patients with age-related maculardegeneration. Experimental Eye Research, 87(5), 445-453.
75. Teunissen, C.E., Van Boxtel, M.P.J., Bosma, H., Bosmans, E., Delanghe, J., De Bruijn, C., ...De Vente, J. (2003). Inflammationmarkers in relation to cognition in a healthy aging population.Journal of Neuroimmunology, 134(1), 142-150.
76. Trachtenberg, A.J., Filippini, N., Ebmeier, K.P., Smith, S.M., Karpe, F., Mackay, C.E. (2012). The effects of APOE on thefunctional architecture of the resting brain. Neuroimage, 59(1), 565-572.
77. Vishwanathan, R., Iannaccone, A., Scott, T.M., Kritchevsky, S.B., Jennings, B.J., Carboni, G., Johnson, E.J. (2014). Macularpigment optical density is related to cognitive function inolder people. Age and Ageing, 43(2), 271-275.
78. Vishwanathan, R., Kuchan, M., Sen, S., Johnson, E. (2014).Lutein and preterm infants with decreased concentrations of braincarotenoids. Journal of Pediatric Gastroenterology and Nutrition, 59(5), 659-665.
79. Vishwanathan, R., Neuringer, M., Snodderly, D.M., Schalch, W., Johnson, E.J. (2013). Macular lutein and zeaxanthin are related tobrain lutein and zeaxanthin in primates. Nutritional Neuroscience, 16(1), 21-29.
80. Wechsler, D. (2001). Wechsler Test of Adult Reading: WTAR. SanAntonio, TX: Psychological Corporation.
81. Wechsler, D. (2009). The Wechsler Memory Scale-Fourth Edition(WMS-IV). San Antonio, TX: Pearson Assessments.
82. Wang, W., Shinto, L., Connor, W.E., Quinn, J.F. (2008).Nutritional biomarkers in Alzheimer's disease: The associationbetween carotenoids, n-3 fatty acids, dementia severity.Journal of Alzheimer's Disease, 13(1), 31-38.
83. Witte, A.V., Kerti, L., Hermannstädter, H.M., Fiebach, J.B., Schreiber, S.J., Schuchardt, J.P., Floël, A. (2014). Longchainomega-3 fatty acids improve brain function and structure inolder adults. Cerebral Cortex, 24(11), 3059-3068.
84. Xie, C., Bai, F., Yu, H., Shi, Y., Yuan, Y., Chen, G., Li, S.(2012). Abnormal insula functional network is associated withepisodic memory decline in amnestic mild cognitive impairment.Neuroimage, 63(1), 320-327.
85. Yesavage, J.A., Brink, T.L., Rose, T.L., Lum, O., Huang, V., Adey, M., Leirer, V.O. (1983). Development and validation ofa geriatric depression screening scale: A preliminary report.Journal of Psychiatric Research, 17(1), 37-49.