Fish oil supplementation increases event-related posterior cingulate activation in older adults with subjective memory impairment

Journal of Nutrition, Health and Aging

Volumn 20, Issue 2, 2016, Pages 161-169

  Boespflug, E L ^a   McNamara, R K ^a   Eliassen, J C ^a   Schidler, M D ^a   Krikorian, Robert ^a  

^a UNIVERSITY OF CINCINNATI ACADEMIC HEALTH CENTER   (United States)

Author keywords

aging; cingulate cortex; functional magnetic resonance imaging; Omega 3 fatty acids; working memory

Indexed keywords

CORN OIL; DOCOSAHEXAENOIC ACID; FISH OIL; ICOSAPENTAENOIC ACID; LONG CHAIN FATTY ACID; OMEGA 3 FATTY ACID; PLACEBO; OXYGEN;

ADULT; AGED; ARTICLE; BLUEBERRY; BOLD SIGNAL; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOUBLE BLIND PROCEDURE; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; INSULA; LIPID COMPOSITION; MALE; MEMORY DISORDER; MIDDLE FRONTAL GYRUS; OUTCOME ASSESSMENT; PARAHIPPOCAMPAL GYRUS; POSTERIOR CINGULATE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SENSORIMOTOR CORTEX; SENSORIMOTOR FUNCTION; SUPERIOR FRONTAL GYRUS; TASK PERFORMANCE; WORKING MEMORY; ANIMAL; BLOOD; DIETARY SUPPLEMENT; DRUG EFFECTS; MEMORY DISORDERS; METABOLISM; MIDDLE AGED; SHORT TERM MEMORY;

AGED; ANIMALS; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; DOUBLE-BLIND METHOD; EICOSAPENTAENOIC ACID; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; FEMALE; FISH OILS; GYRUS CINGULI; HUMANS; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; MIDDLE AGED; OXYGEN;

EID: 84957846176     PISSN: 12797707     EISSN: 17604788     Source Type: Journal    
DOI: 10.1007/s12603-015-0609-6     Document Type: Article

References (59)

1. Imtiaz B, Tolppanen AM, Kivipelto M, Soininen H. Future directions in Alzheimer’s disease from risk factors to prevention. Biochem Pharmacol. 2014;88:661–670.
2. Solomon A, Mangialasche F, Richard E, Andrieu S, Bennett DA, Breteler M, Fratiglioni L, Hooshmand B, Khachaturian AS, Schneider LS, Skoog I, Kivipelto M. Advances in the prevention of Alzheimer’s disease and dementia. J Intern Med. 2014;275:229–250.
3. Jessen F, Wiese B, Bachmann C, Eifflaender-Gorfer S, Haller F, Kölsch H, Luck T, Mösch E, van den Bussche H, Wagner M, Wollny A, Zimmermann T, Pentzek M, Riedel-Heller SG, Romberg HP, Weyerer S, Kaduszkiewicz H, Maier W, Bickel H. Prediction of dementia by subjective memory impairment: effects of severity and temporal association with cognitive impairment. Arch Gen Psychiatry. 2010;67:414–422.
4. Rönnlund M, Sundström A, Adolfsson R, Nilsson LG. Subjective memory impairment in older adults predicts future dementia independent of baseline memory performance: Evidence from the Betula prospective cohort study. Alzheimers Dement. [Epub ahead of print]. 2015 5.
5. Waldorff FB, Siersma V, Vogel A, Waldemar G. Subjective memory complaints in general practice predicts future dementia: a 4-year follow-up study. Int J Geriatr Psychiatry. 2012;27:1180–1188.
6. Meiberth D, Scheef L, Wolfsgruber S, Boecker H, Block W, Träber F, Erk S, Heneka MT, Jacobi H, Spottke A, Walter H, Wagner M, Hu X, Jessen F. Cortical thinning in individuals with subjective memory impairment. J Alzheimers Dis. 2015;45:139–146.
7. Saykin AJ, Wishart HA, Rabin LA, Santulli RB, Flashman LA, West JD, Mc Hugh TL, Mamourian AC. Older adults with cognitive complaints show brain atrophy similar to that of amnestic MCI. Neurology. 2006;67:834–842.
8. Schultz SA, Oh JM, Koscik RL, Dowling NM, Gallagher CL, Carlsson CM, Bendlin BB, La Rue A, Hermann BP, Rowley HA, Asthana S, Sager MA, Johnson SC, Okonkwo OC. Subjective memory complaints, cortical thinning, and cognitive dysfunction in middle-aged adults at risk for AD. Alzheimers Dement (Amst). 2015;1:33–40.
9. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR et al. Toward defining the preclinical stages of Alzheimer’s disease. Alzheimers Dementia, 2011;7:280–292.
10. Lista S, Dubois B, Hampel H. Paths to Alzheimer’s disease prevention: from modifiable risk factors to biomarker enrichment strategies. J Nutr Health Aging. 2015;19:154–163.
11. Barberger-Gateau P, Raffaitin C, Letenneur L, Berr C, Tzourio C, Dartigues JF, Alpérovitch A. Dietary patterns and risk of dementia: the Three-City cohort study. Neurology. 2007;69:1921–1930.
12. Heude B, Ducimetière P, Berr C; EVA Study. Cognitive decline and fatty acid composition of erythrocyte membranes—The EVA Study. Am J Clin Nutr. 2003;77:803–808.
13. Kalmijn S, van Boxtel MP, Ocké M, Verschuren WM, Kromhout D, Launer LJ. Dietary intake of fatty acids and fish in relation to cognitive performance at middle age. Neurology. 2004;62:275–280.
14. Morris MC, Evans DA, Bienias JL, Tangney CC, Bennett DA, Wilson RS, Aggarwal N, Schneider J. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch Neurol. 2003;60:940–946.
15. Schaefer EJ, Bongard V, Beiser AS, Lamon-Fava S, Robins SJ, Au R, Tucker KL, Kyle DJ, Wilson PW, Wolf PA. Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: the Framingham Heart Study. Arch Neurol. 2006;63:1545–1550.
16. Sands SA, Reid KJ, Windsor SL, Harris WS. The impact of age, body mass index, and fish intake on the EPA and DHA content of human erythrocytes. Lipids. 2005;40:343–347.
17. Lin PY, Chiu CC, Huang SY, Su KP. A meta-analytic review of polyunsaturated fatty acid compositions in dementia. J Clin Psychiatry. 2012;73:1245–1254.
18. Conklin SM, Gianaros PJ, Brown SM, Yao JK, Hariri AR, Manuck SB, Muldoon MF. Long-chain omega-3 fatty acid intake is associated positively with corticolimbic gray matter volume in healthy adults. Neurosci Lett. 2007;421:209–212.
19. Pottala JV, Yaffe K, Robinson JG, Espeland MA, Wallace R, Harris WS. Higher RBC EPA + DHA corresponds with larger total brain and hippocampal volumes: WHIMS-MRI study. Neurology. 2014;82:435–442.
20. Raji CA, Erickson KI, Lopez OL, Kuller LH, Gach HM, Thompson PM, Riverol M, Becker JT. Regular fish consumption and age-related brain gray matter loss. Am J Prev Med. 2014;47:444–451.
21. Samieri C, Maillard P, Crivello F, Proust-Lima C, Peuchant E, Helmer C, Amieva H, Allard M, Dartigues JF, Cunnane SC, Mazoyer BM, Barberger-Gateau P. Plasma long-chain omega-3 fatty acids and atrophy of the medial temporal lobe. Neurology. 2012;79:642–650.
22. Tan ZS, Harris WS, Beiser AS, Au R, Himali JJ, Debette S, Pikula A, Decarli C, Wolf PA, Vasan RS, Robins SJ, Seshadri S. Red blood cell -3 fatty acid levels and markers of accelerated brain aging. Neurology. 2012;78:658–664.
23. Titova OE, Sjögren P, Brooks SJ, Kullberg J, Ax E, Kilander L, Riserus U, Cederholm T, Larsson EM, Johansson L, Ahlström H, Lind L, Schiöth HB, Benedict C. Dietary intake of eicosapentaenoic and docosahexaenoic acids is linked to gray matter volume and cognitive function in elderly. Age (Dordr). 2013;35:1495–1505.
24. Walhovd KB, Storsve AB, Westlye LT, Drevon CA, Fjell AM. Blood markers of fatty acids and vitamin D, cardiovascular measures, body mass index, and physical activity relate to longitudinal cortical thinning in normal aging. Neurobiol Aging. 35:1055-1064.
25. 2014;Witte AV, Kerti L, Hermannstädter HM, Fiebach JB, Schreiber SJ, Schuchardt JP, Hahn A, Flöel A. Long-chain omega-3 fatty acids improve brain function and structure in older adults. Cereb Cortex. 2014;24:3059–3068.
26. Quinn JF, Raman R, Thomas RG, Yurko-Mauro K, Nelson EB, Van Dyck C, Galvin JE, Emond J, Jack CR Jr, Weiner M, Shinto L, Aisen PS. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA. 200;304:1903-1911.
27. Arai H, Takano M, Miyakawa K, Ota T, Takahashi T, Asaka H, Kawaguchi T. A quantitative near-infrared spectroscopy study: a decrease in cerebral hemoglobin oxygenation in Alzheimer’s disease and mild cognitive impairment. Brain Cogn. 2006;61:189–194.
28. Hock C, Villringer K, Müller-Spahn F, Hofmann M, Schuh-Hofer S, Heekeren H, Wenzel R, Dirnagl U, Villringer A. Near infrared spectroscopy in the diagnosis of Alzheimer’s disease. Ann N Y Acad Sci. 1996;777:22–29.
29. Zeller JB, Herrmann MJ, Ehlis AC, Polak T, Fallgatter AJ. Altered parietal brain oxygenation in Alzheimer’s disease as assessed with near-infrared spectroscopy. Am J Geriatr Psychiatry. 2010;18:433–441.
30. Pu S, Nakagome K, Yamada T, Matsumura H, Yokoyama K, Kaneko K, Kurosawa Y. Association between fish consumption and prefrontal function during a cognitive task in male Japanese workers: A multi-channel near-infrared spectroscopy study. PLoS One. 2015;10:e0123972.
31. Jackson PA, Reay JL, Scholey AB, Kennedy DO. DHA-rich oil modulates the cerebral haemodynamic response to cognitive tasks in healthy young adults: a near IR spectroscopy pilot study. Br J Nutr. 2012;107:1093–1098.
32. McNamara RK, Able J, Jandacek R, Rider T, Tso P, Eliassen JC, Alfieri D, Weber W, Jarvis K, DelBello MP, Strakowski SM, Adler CM. Docosahexaenoic acid supplementation increases prefrontal cortex activation during sustained attention in healthy boys: a placebo-controlled, dose-ranging, functional magnetic resonance imaging study. Am J Clin Nutr. 2010;91:1060–1067.
33. Bauer I, Hughes M, Rowsell R, Cockerell R, Pipingas A, Crewther S, Crewther D. Omega-3 supplementation improves cognition and modifies brain activation in young adults. Hum Psychopharmacol. 2014;29:133–144.
34. Krikorian R, Zimmerman ME, Fleck DE. Inhibitory control in Obsessive-Compulsive Disorder. Brain Cognit. 2004;54:257–259.
35. Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL. A new clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566–572.
36. Boake EC. Claparede and the Auditory Verbal Learning Test. J Clin Exp Neuropsychol. 2000;22:286–292.
37. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO. Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res. 1983;17:37–49.
38. Freund-Levi Y, Eriksdotter-Jönhagen M, Cederholm T, Basun H, Faxén- Irving G, Garlind A, Vedin I, Vessby B, Wahlund LO, Palmblad J. Omega-3 fatty acid treatment in 174 patients with mild to moderate Alzheimer disease: OmegAD study: a randomized double-blind trial. Arch Neurol. 2006;63:1402–1408.
39. Schmithorst VJ, Dardzinski BJ, Holland SK. Simultaneous correction of ghost and geometric distortion artifacts in EPI using a multiecho reference scan. IEEE Trans Med Imaging. 2001;20:535–539.
40. Lee JH, Garwood M, Menon R, Adriany G, Andersen P, Truwit CL, Ugurbil K. High contrast and fast three-dimensional magnetic resonance imaging at high fields. Magn Reson Med. 1995;34:308–312.
41. Owen AM, Mc Millan KM, Laird AR, Bullmore E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp. 2005;25:46–59.
42. Yetkin FZ, Rosenberg RN, Weiner MF, Purdy PD, Cullum CM. FMRI of working memory in patients with mild cognitive impairment and probable Alzheimer’s disease. Eur Radiol. 2006;16:193–206.
43. Cox RW. AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comp. Biomed. Res. 1996;29:162–173.
44. Chen G, Adleman NE, Saad ZS, Leibenluft E, Cox RW. Applications of multivariate modeling to neuroimaging group analysis: a comprehensive alternative to univariate general linear model. Neuroimage. 2014;99:571–588.
45. Janssen CI, Kiliaan AJ. Long-chain polyunsaturated fatty acids (LCPUFA) from genesis to senescence: the influence of LCPUFA on neural development, aging, and neurodegeneration. Prog Lipid Res. 2014;53:1–17.
46. Cox RW, Jesmanowicz A. Real-time 3D image registration for functional MRI. Magn. Reson. Med. 1999;42:1014–1018.
47. Krikorian R, Boespflug EL, Fleck DE, Stein AL, Wightman JD, Shidler MD, Sadat-Hossieny S. Concord grape juice supplementation and neurocognitive function in human aging. J Agric Food Chem. 60:5736-5742.
48. Rapoport SI, Ramadan E, Basselin M. Docosahexaenoic acid (DHA) incorporation into the brain from plasma, as an in vivo biomarker of brain DHA metabolism and neurotransmission. Prostaglandins Other Lipid Mediat. 2011;96:109–113.
49. McNamara RK, Liu Y, Jandacek R, Rider T, Tso P. The aging human orbitofrontal cortex: decreasing polyunsaturated fatty acid composition and associated increases in lipogenic gene expression and stearoyl-CoA desaturase activity. Prostaglandins Leukot Essent Fatty Acids. 2008;78:293–304.
50. Smesny S, Milleit B, Hipler UC, Milleit C, Schäfer MR, Klier CM, Holub M, Holzer I, Berger GE, Otto M, Nenadic I, Berk M, Mc Gorry PD, Sauer H, Amminger GP. Omega-3 fatty acid supplementation changes intracellular phospholipase A2 activity and membrane fatty acid profiles in individuals at ultra-high risk for psychosis. Mol Psychiatry. 2014;19:317–324.
51. Gattaz WF, Cairns NJ, Levy R, Förstl H, Braus DF, Maras A. Decreased phospholipase A2 activity in the brain and in platelets of patients with Alzheimer’s disease. Eur Arch Psychiatry Clin Neurosci. 1996;246:129–131.
52. Gattaz WF, Forlenza OV, Talib LL, Barbosa NR, Bottino CM. Platelet phospholipase A(2) activity in Alzheimer’s disease and mild cognitive impairment. J Neural Transm. 2004;111:591–601.
53. Ross BM, Moszczynska A, Erlich J, Kish SJ. Phospholipid-metabolizing enzymes in Alzheimer’s disease: increased lysophospholipid acyltransferase activity and decreased phospholipase A2 activity. J Neurochem. 1998;70:786–793.
54. Smesny S, Stein S, Willhardt I, Lasch J, Sauer H. Decreased phospholipase A2 activity in cerebrospinal fluid of patients with dementia. J Neural Transm. 2008;115:1173–1179.
55. Talbot K, Young RA, Jolly-Tornetta C, Lee VM, Trojanowski JQ, Wolf BA. A frontal variant of Alzheimer’s disease exhibits decreased calcium-independent phospholipase A2 activity in the prefrontal cortex. Neurochem Int. 2000;37:17–31.
56. Zamroziewicz, MK, Paul EJ, Rubin RD, Barbey AK. Anterior cingulate cortex mediates the relationship between O3PUFAs and executive functions in APOE e4 carriers. Front Aging Neurosci. 2015;7:87.
57. Beckmann M, Johansen-Berg H, Rushworth MF. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci. 2009;29:1175–1190.
58. Francis ST, Head K, Morris PG, Macdonald IA. The effect of flavanol-rich cocoa on the fMRI response to a cognitive task in healthy young people. J Cardiovasc Pharmacol. 2006;47:S215–S220.
59. Krikorian R, Eliassen JC, Boespflug EL, Nash TA, Shidler MD. Improved cognitivecerebral function in older adults with chromium supplementation. Nutr. Neurosci. 2010;13:116–122.