Nutritional status, brain network organization, and general intelligence

NeuroImage

Volumn 161, Issue , 2017, Pages 241-250

  Zamroziewicz, Marta K ^a   Talukdar, M Tanveer ^a   Zwilling, Chris E ^a   Barbey, Aron K ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b CARLE FOUNDATION HOSPITAL   (United States)

Author keywords

Functional connectivity; General intelligence; Monounsaturated fatty acids; Nutritional cognitive neuroscience; Saturated fatty acids

Indexed keywords

MONOUNSATURATED FATTY ACID; SATURATED FATTY ACID;

ADULT; AGED; ARTICLE; BRAIN SIZE; DECISION MAKING; DORSAL ATTENTION NETWORK; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INTELLIGENCE; MALE; MEDITERRANEAN DIET; MENTAL PERFORMANCE; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; NUTRIENT; NUTRITIONAL STATUS; PRIORITY JOURNAL; ATTENTION; BLOOD; BRAIN; CONNECTOME; CROSS-SECTIONAL STUDY; DIAGNOSTIC IMAGING; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; STATISTICAL MODEL;

AGED; ATTENTION; BRAIN; CONNECTOME; CROSS-SECTIONAL STUDIES; FATTY ACIDS, MONOUNSATURATED; FEMALE; HUMANS; INTELLIGENCE; MAGNETIC RESONANCE IMAGING; MALE; MODELS, STATISTICAL; NERVE NET; NUTRITIONAL STATUS;

EID: 85028974953     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2017.08.043     Document Type: Article

References (101)

1. Aranceta, J., Pérez-Rodrigo, C., Recommended dietary reference intakes, nutritional goals and dietary guidelines for fat and fatty acids: a systematic review. Br. J. Nutr. 107:S2 (2012 Jun 17), S8–S22.
2. Aryen, J.J., Julkunen, A., Penttila, I., Rapid separation of serum lipids for fatty acid analysis by a single aminopropyl column. J. Lipid Res. 33 (1992), 1871–1876.
3. Auerbach, E.J., Xu, J., Yacoub, E., Moeller, S., Uğurbil, K., Multiband accelerated spin-echo echo planar imaging with reduced peak RF power using time-shifted RF pulses. Magn. Reson Med. 69:5 (2013 May), 1261–1267.
4. Babyak, M.A., What You See May Not Be What You Get: A Brief, Nontechnical Introduction to Overfitting in Regression-Type Models. Psychosom. Med. 66:3 (2004 May 1), 411–421.
5. Barbey, A.K., Colom, R., Solomon, J., Krueger, F., Forbes, C., Grafman, J., An integrative architecture for general intelligence and executive function revealed by lesion mapping. Brain 135:4 (2012 Apr 1), 1154–1164.
6. Barbey, A.K., Colom, R., Grafman, J., Dorsolateral prefrontal contributions to human intelligence. Neuropsychologia 51:7 (2013 Jun), 1361–1369.
7. Barbey, A.K., Colom, R., Grafman, J., Architecture of cognitive flexibility revealed by lesion mapping. Neuroimage 82 (2013 Nov), 547–554.
8. Barbey, A.K., Colom, R., Paul, E.J., Grafman, J., Architecture of fluid intelligence and working memory revealed by lesion mapping. Brain Struct. Funct. 219:2 (2014 Mar 8), 485–494.
9. Bartlett, M.S., Tests of significance in factor analysis. Br. J. Math. Stat. Psychol. 3 (1950), 77–85.
10. Beckmann, C.F., DeLuca, M., Devlin, J.T., Smith, S.M., Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. 360 (2005), 1001–1013.
11. Benjamini, Y., Hochberg, Y., Controlling the false discovery Rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57:1 (1995), 289–300.
12. Berti, V., Murray, J., Davies, M., Spector, N., Tsui, W.H., Li, Y., et al. Nutrient patterns and brain biomarkers of Alzheimer's disease in cognitively normal individuals. J. Nutr. Health Aging 19:4 (2015), 413–423.
13. Bobko, P., Correlation and Regression: Applications for Industrial Organizational Psychology and Management. 2001, Sage Publications, Inc.
14. Boespflug, E.L., McNamara, R.K., Eliassen, J.C., Schidler, M.D., Krikorian, R., Fish oil supplementation increases event-related posterior cingulate activation in older adults with subjective memory impairment. J. Nutr. Health Aging 20:2 (2016 Feb 24), 161–169.
15. Bowman, G.L., Silbert, L.C., Howieson, D., Dodge, H.H., Traber, M.G., Frei, B., et al. Nutrient biomarker patterns, cognitive function, and MRI measures of brain aging. Neurology 78:4 (2012), 241–249.
16. Bowman, G.L., Dodge, H.H., Mattek, N., Barbey, A.K., Silbert, L.C., Shinto, L., et al. Plasma omega-3 PUFA and white matter mediated executive decline in older adults. Front. Aging Neurosci. 5:DEC (2013), 1–7.
17. Bullmore, E., Sporns, O., Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Publ. Gr 10:3 (2009), 186–198.
18. Clarke, D.D., Sokoloff, L., Circulation and Energy Metabolism of the brain. Siegel, G., Agranoff, B., Albers, R., (eds.) Basic Neurochemistry: Molecular, Cellular, and Medical Aspects, sixth ed., 1999, Lippincott-Raven, Philadelphia.
19. Colom, R., Karama, S., Jung, R.E., Haier, R.J., Human intelligence and brain networks. Dialogues Clin. Neurosci. 12 (2010), 489–501.
20. Craddock, R.C., James, G.A., Holtzheimer, P.E., Hu, X.P., Mayberg, H.S., A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum. Brain Mapp. 33:8 (2012 Aug), 1914–1928.
21. Crane, P.K., Walker, R., Hubbard, R.A., Li, G., Nathan, D.M., Zheng, H., et al. Glucose levels and risk of dementia. N. Engl. J. Med. 369:6 (2013), 540–548.
22. Damoiseaux, J.S., Effects of aging on functional and structural brain connectivity. Neuroimage, 2017.
23. Damoiseaux, J.S., Rombouts, S.A.R.B., Barkhof, F., Scheltens, P., Stam, C.J., Smith, S.M., et al. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 103:37 (2006), 13848–13853.
24. Deary, I.J., Penke, L., Johnson, W., The neuroscience of human intelligence differences. Nat. Rev. Neurosci. 11 (2010), 201–211.
25. Dumas, J.A., Bunn, J.Y., Nickerson, J., Crain, K.I., Ebenstein, D.B., Tarleton, E.K., et al. Dietary saturated fat and monounsaturated fat have reversible effects on brain function and the secretion of pro-inflammatory cytokines in young women. Metabolism 65:10 (2016), 1582–1588.
26. Duncan, J., Seitz, R.J., Kolodny, J., Bor, D., Herzog, H., Ahmed, A., et al. A neural basis for general intelligence. Sci. (80- ) 289 (2000), 457–460.
27. Dyson, P.A., Kelly, T., Deakin, T., Duncan, A., Frost, G., Harrison, Z., et al. Diabetes UK evidence-based nutrition guidelines for the prevention and management of diabetes. Diabet. Med. 28 (2011), 1282–1288.
28. Esposito, K., Marfella, R., Ciotola, M., Di, Palo C., Giugliano, F., Giugliano, G., et al. Effect of a mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial. JAMA 292:12 (2004), 1440–1446.
29. Evert, A.B., Boucher, J.L., Cypress, M., Dunbar, S.A., Franz, M.J., Mayer-Davis, E.J., et al. Nutrition therapy recommendations for the management of adults with diabetes. Diabetes Care 36 (2013), 3821–3842.
30. Feart, C., Samieri, C., Barberger-Gateau, P., Mediterranean diet and cognitive health: an update of available knowledge. Curr. Opin. Clin. Nutr. Metab. Care 18:1 (2015), 51–62.
31. Folch, J., Lees, M., Sloane Stanley, G.H., A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226 (1957), 497–509.
32. Folstein, M.F., Folstein, S.E., McHugh, P.R., “Mini-mental state” A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12:3 (1975), 189–198.
33. Fox, M.D., Zhang, D., Snyder, A.Z., Raichle, M.E., The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 101:6 (2009 Jun 1), 3270–3283.
34. Gallucci, M., Mazzuco, S., Ongaro, F., Di Giorgi, E., Mecocci, P., Cesari, M., et al. Body mass index, lifestyles, physical performance and cognitive decline: the “Treviso Longeva (TRELONG)” study. J. Nutr. Heal Aging 17:4 (2013), 378–384.
35. Gottfredson, L.S., Why g matters: the complexity of everyday life. Intelligence 24:1 (1997), 79–132.
36. Goyal, M.S., Venkatesh, S., Milbrandt, J., Gordon, J.I., Raichle, M.E., Feeding the brain and nurturing the mind: linking nutrition and the gut microbiota to brain development. Proc. Natl. Acad. Sci. 112:46 (2015 Nov 17), 14105–14112.
37. Grady, C., Sarraf, S., Saverino, C., Campbell, K., Age differences in the functional interactions among the default, frontoparietal control, and dorsal attention networks. Neurobiol. Aging 41 (2016), 159–172.
38. Gu, Y., Vorburger, R.S., Gazes, Y., Habeck, C.G., Stern, Y., Luchsinger, J.A., et al. White matter integrity as a mediator in the relationship between dietary nutrients and cognition in the elderly. Ann. Neurol. 79:6 (2016 Jun), 1014–1025.
39. Hardman, R.J., Kennedy, G., Macpherson, H., Scholey, A.B., Pipingas, A., Adherence to a mediterranean-style diet and effects on cognition in adults: a qualitative evaluation and systematic review of longitudinal and prospective trials. Front. Nutr. 3:22 (2016), 1–13.
40. Hearne, L.J., Mattingley, J.B., Cocchi, L., Functional brain networks related to individual differences in human intelligence at rest. Sci. Rep. 6:32328 (2016), 1–8.
41. Hurst, L., Stafford, M., Cooper, R., Hardy, R., Richards, M., Kuh, D., Lifetime socioeconomic inequalities in physical and cognitive aging. Am. J. Public Health 103:9 (2013 Sep), 1641–1648.
42. Jenkinson, M., Beckmann, C.F., Behrens, T.E.J., Woolrich, M.W., Smith, S.M., FSL. Neuroimage 62:2 (2012 Aug), 782–790.
43. Jolliffe, I., Principal Component Analysis. 2014, Wiley StatsRef.
44. Kaiser, H.F., A second generation little jiffy. Psychometrika 35:4 (1970), 401–415.
45. Koen, J.D., Yonelinas, A.P., The effects of healthy aging, amnestic mild cognitive impairment, and Alzheimer's disease on recollection and familiarity: a meta-analytic review. Neuropsychol. Rev. 24:3 (2014 Sep 15), 332–354.
46. Konagai, C., Yanagimoto, K., Hayamizu, K., Li, H., Tsuji, T., Koga, Y., Effects of krill oil containing n-3 polyunsaturated fatty acids in phospholipid form on human brain function: a randomized controlled trial in healthy elderly volunteers. Clin. Interv. Aging 8 (2013), 1247–1257.
47. Laird, A.R., Fox, P.M., Eickhoff, S.B., Turner, J.A., Ray, K.L., McKay, D.R., et al. Behavioral interpretations of intrinsic connectivity networks. J. Cogn. Neurosci. 23:12 (2011), 4022–4037.
48. Lowe, M.J., Mock, B.J., Sorenson, J.A., Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7:2 (1998 Feb), 119–132.
49. Lynn, R., The role of nutrition in secular increases in intelligence. Pers. Individ. Dif. 11:3 (1990), 273–285.
50. Manschot, S.M., Brands, A.M.A., van der Grond, J., Kessels, R.P.C., Algra, A., Kappelle, L.J., et al. Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes 55 (2006), 1106–1113.
51. Matthews, D.C., Davies, M., Murray, J., Williams, S., Tsui, W.H., Li, Y., et al. Physical activity, mediterranean diet and biomarkers-assessed risk of Alzheimer's: a multi-modality brain imaging study. Adv. Mol. Imaging 4:4 (2014), 43–57.
52. Mennes, M., Vega Potler, N., Kelly, C., Di Martino, A., Castellanos, F.X., Milham, M.P., Resting state functional connectivity correlates of inhibitory control in children with attention-deficit/hyperactivity disorder. Front. Psychiatry 2:JAN (2012), 1–17.
53. Morrison, W.R., Smith, L.M., Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J. Lipid Res. 55 (1964), 600–608.
54. Muldoon, S.F., Bridgeford, E.W., Bassett, D.S., Small-world propensity and weighted brain networks. Sci. Rep. 6:22057 (2016), 1–13.
55. Murphy, K., Birn, R.M., Handwerker, D.A., Jones, T.B., Bandettini, P.A., The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. Neuroimage 44:3 (2009 Feb), 893–905.
56. Musen, G., Jacobson, A.M., Bolo, N.R., Simonson, D.C., Shenton, M.E., McCartney, R.L., et al. Resting-state brain functional connectivity is altered in type 2 diabetes. Diabetes 61 (2012), 2375–2379.
57. Osborne, J.W., Costello, A.B., Sample size and subject to item ratio in principal components analysis. Osborne, Jason W. & Anna B. Costello. Pract Assessment. Res. Eval. 9:11 (2004), 1–9.
58. Pamplona, G.S.P., Santos Neto, G.S., Rosset, S.R.E., Rogers, B.P., Salmon, C.E.G., Analyzing the association between functional connectivity of the brain and intellectual performance. Front. Hum. Neurosci. 9:February (2015), 1–11.
59. Pauls, F., Petermann, F., Lepach, A.C., Gender differences in episodic memory and visual working memory including the effects of age. Memory 21:7 (2013 Oct), 857–874.
60. Power, J.D., Barnes, K.A., Snyder, A.Z., Schlaggar, B.L., Petersen, S.E., Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:3 (2012 Feb), 2142–2154.
61. Preacher, K.J., Hayes, A.F., Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav. Res. Methods 40:3 (2008), 879–891.
62. Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L., A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 98:2 (2001), 676–682.
63. Rönnlund, M., Nyberg, L., Bäckman, L., Nilsson, L.-G., Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychol. Aging 20:1 (2005), 3–18.
64. Samieri, C., Grodstein, F., Rosner, B.A., Kang, J.H., Cook, N.R., Manson, J.E., et al. Mediterranean diet and cognitive function in older age: results from the Women's Health Study. Epidemiology 24:4 (2013), 490–499.
65. Santarnecchi, E., Tatti, E., Rossi, S., Serino, V., Rossi, A., Intelligence-related differences in the asymmetry of spontaneous cerebral activity. Hum. Brain Mapp. 36 (2015), 3586–3602.
66. Sartorius, T., Ketterer, C., Kullmann, S., Balzer, M., Rotermund, C., Binder, S., et al. Monounsaturated fatty acids prevent the aversive effects of obesity on locomotion, brain activity, and sleep behavior. Diabetes 61:7 (2012), 1669–1679.
67. Satterthwaite, T.D., Wolf, D.H., Loughead, J., Ruparel, K., Elliott, M.A., Hakonarson, H., et al. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 60:1 (2012 Mar), 623–632.
68. Shai, I., Schwarzfuchs, D., Henkin, Y., Shahar, D.R., Witkow, S., Greenberg, I., et al. Weight loss with a low-carbohydrate, Mediterranean, or low-fat diet. N. Engl. J. Med. 359:3 (2008), 229–241.
69. Smith, S.M., Fast robust automated brain extraction. Hum. Brain Mapp. 17:3 (2002), 143–155.
70. Smith, S.M., Nichols, T.E., Vidaurre, D., Winkler, A.M., Behrens, T.E., Glasser, M.F., et al. A positive-negative mode of population covariation links brain connectivity, demographics and behavior. Nat. Neurosci. 18:11 (2015), 1565–1567.
71. Solfrizzi, V., Panza, F., Torres, F., Mastroianni, F., Del Parigi, A., Venezia, A., et al. High monounsaturated fatty acids intake protects against age-related cognitive decline. Neurology, 52(8), 1999 May 1 1563–1563.
72. Solfrizzi, V., Colacicco, A.M., D'Introno, A., Capurso, C., Torres, F., Rizzo, C., et al. Dietary intake of unsaturated fatty acids and age-related cognitive decline: a 8.5-year follow-up of the Italian Longitudinal Study on Aging. Neurobiol. Aging 27:11 (2006), 1694–1704.
73. Song, M., Zhou, Y., Li, J., Liu, Y., Tian, L., Yu, C., et al. Brain spontaneous functional connectivity and intelligence. Neuroimage 41:3 (2008), 1168–1176.
74. Song, M., Liu, Y., Zhou, Y., Wang, K., Yu, C., Jiang, T., Default network and intelligence difference. IEE Trans. Auton. Ment. Dev. 1:2 (2009), 101–109.
75. Sporns, O., Zwi, J.D., The small world of the cerebral cortex. Neuroinformatics 2:2 (2004), 145–162.
76. Spreng, R.N., Sepulcre, J., Turner, G.R., Stevens, W.D., Schacter, D.L., Intrinsic architecture underlying the relations among the default, dorsal attention, and frontoparietal control networks of the human brain. J. Cogn. Neurosci. 25:1 (2013), 74–86.
77. Staubo, S.C., Aakre, J.A., Vemuri, P., Syrjanen, J.A., Mielke, M.M., Geda, Y.E., et al. Mediterranean diet, micronutrients and macronutrients, and MRI measures of cortical thickness. Alzheimer's Dement. 13:2 (2017 Feb), 168–177.
78. Strenze, T., Intelligence and socioeconomic success: a meta-analytic review of longitudinal research. Intelligence 35 (2007), 401–426.
79. Tabachnick, B.G., Fidell, L.S., Using Multivariate Statistics. fifth ed., 2007, Pearson Allyn & Bacon, Upper Saddle River, NJ, 646.
80. van den Heuvel, M.P., Stam, C.J., Boersma, M., Hulshoff Pol, H.E., Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain. Neuroimage 43 (2008), 528–539.
81. Van Dijk, K.R.A., Hedden, T., Venkataraman, A., Evans, K.C., Lazar, S.W., Buckner, R.L., Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 103:1 (2010 Jan 1), 297–321.
82. Vessby, B., Uusitupa, M., Hermansen, K., Riccardi, G., Rivellese, A.A., Tapsell, L.C., et al. Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU study. Diabetologia 44 (2001), 312–319.
83. Wang, L., Song, M., Jiang, T., Zhang, Y., Yu, C., Regional homogeneity of the resting-state brain activity correlates with individual intelligence. Neurosci. Lett. 488:3 (2011), 275–278.
84. Ware, J.E., Snow, K., Kosinski, M., Gandek, B., Manual and Interpretation Guide. 1993, The Health Institute, New England Medical Center, Boston.
85. Watts, D.J., Strogatz, S.H., Collective dynamics of “small-world” networks. Nature 393:4 (1998), 440–442.
86. Wechsler, D., Wechsler abbreviated scale of intelligence. Psychol. Corp., 1999.
87. Whalley, L.J., Fox, H.C., Wahle, K.W., Starr, J.M., Deary, I.J., Cognitive aging, childhood intelligence, and the use of food supplements: possible involvement of n-3 fatty acids. Am. J. Clin. Nutr. 80 (2004), 1650–1657.
88. Wiesmann, M., Zerbi, V., Jansen, D., Haast, R., Lütjohann, D., Broersen, L.M., et al. A dietary treatment improves cerebral blood flow and brain connectivity in aging apoE4 mice. Neural Plast., 2016, 1–15.
89. Wilkins, V.M., Kiosses, D., Ravdin, L.D., Late-life depression with comorbid cognitive impairment and disability: nonpharmacological interventions. Clin. Interv. Aging 5 (2010 Nov), 323–331.
90. Witte, A.V., Kerti, L., Hermannstädter, H.M., Fiebach, J.B., Schreiber, S.J., Schuchardt, J.P., et al. Long-chain Omega-3 fatty acids improve brain function and structure in older adults. Cereb. Cortex 24:11 (2014 Nov 1), 3059–3068.
91. Xia, W., Wang, S., Rao, H., Spaeth, A.M., Wang, P., Yang, Y., et al. Disrupted resting-state attentional networks in T2DM patients. Sci. Rep. 5:11148 (2015), 1–10.
92. Yeo, B.T.T., Krienen, F.M., Sepulcre, J., Sabuncu, M.R., Lashkari, D., Hollinshead, M., et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106:3 (2011 Sep 1), 1125–1165.
93. Yuan, Z., Qin, W., Wang, D., Jiang, T., Zhang, Y., Yu, C., The salience network contributes to an individual's fluid reasoning capacity. Behav. Brain Res. 229 (2012), 384–390.
94. Zamroziewicz, M.K., Barbey, A.K., Nutritional cognitive neuroscience: innovations for healthy brain aging. Front. Neurosci. 10:240 (2016), 1–10.
95. Zamroziewicz, M.K., Paul, E.J., Rubin, R.D., Barbey, A.K., Anterior cingulate cortex mediates the relationship between O3PUFAs and executive functions in APOE e4 carriers. Front. Aging Neurosci. 7:87 (2015), 1–7.
96. Zamroziewicz, M.K., Paul, E.J., Zwilling, C.E., Johnson, E.J., Kuchan, M.J., Cohen, N.J., et al. Parahippocampal cortex mediates the relationship between lutein and crystallized intelligence in healthy, older adults. Front. Aging Neurosci. 8:297 (2016), 1–9.
97. Zamroziewicz, M.K., Zwilling, C.E., Barbey, A.K., Inferior prefrontal cortex mediates the relationship between phosphatidylcholine and executive functions in healthy, older adults. Front. Aging Neurosci. 8:226 (2016), 1–8.
98. Zamroziewicz, M.K., Paul, E.J., Zwilling, C.E., Barbey, A.K., Determinants of fluid intelligence in healthy aging: omega-3 polyunsaturated fatty acid status and frontoparietal cortex structure. Nutr Neurosci., 2017 May 11, 1–10.
99. Zamroziewicz, M.K., Paul, E.J., Zwilling, C.E., Barbey, A.K., Predictors of memory in healthy aging: polyunsaturated fatty acid balance and fornix white matter integrity. Aging Dis. 9:1 (2018), 1–12.
100. Zhang, Y., Brady, M., Smith, S., Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 20:1 (2001), 45–57.
101. Zhao, X., Lynch, J.G., Chen, Q., Reconsidering baron and Kenny: myths and truths about mediation analysis. J. Consum. Res. 37:2 (2010 Aug), 197–206.