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Predictors of Memory in Healthy Aging: Polyunsaturated Fatty Acid Balance and Fornix White Matter Integrity
Marta K. Zamroziewicz1,2,3, Erick J. Paul 1,2, Chris E. Zwilling1,2, Aron K. Barbey1,2,3,4,5,6,7,*
1Decision Neuroscience Laboratory, University of Illinois Urbana-Champaign, Urbana, IL, USA.
2Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, IL, USA.
3Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, IL, USA.
4Department of Psychology, University of Illinois Urbana-Champaign, Urbana, IL, USA.
5Carle Neuroscience Institute, Carle Foundation Hospital, Urbana, IL, USA.
6Department of Internal Medicine, University of Illinois Urbana-Champaign, Urbana, IL, USA.
7Institute for Genomic Biology, University of Illinois Urbana-Champaign, Champaign, IL, USA
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Abstract  

Recent evidence demonstrates that age and disease-related decline in cognition depends not only upon degeneration in brain structure and function, but also on dietary intake and nutritional status. Memory, a potential preclinical marker of Alzheimer’s disease, is supported by white matter integrity in the brain and dietary patterns high in omega-3 and omega-6 polyunsaturated fatty acids. However, the extent to which memory is supported by specific omega-3 and omega-6 polyunsaturated fatty acids, and the degree to which this relationship is reliant upon microstructure of particular white matter regions is not known. This study therefore examined the cross-sectional relationship between empirically-derived patterns of omega-3 and omega-6 polyunsaturated fatty acids (represented by nutrient biomarker patterns), memory, and regional white matter microstructure in healthy, older adults. We measured thirteen plasma phospholipid omega-3 and omega-6 polyunsaturated fatty acids, memory, and regional white matter microstructure in 94 cognitively intact older adults (65 to 75 years old). A three-step mediation analysis was implemented using multivariate linear regressions, adjusted for age, gender, education, income, depression status, and body mass index. The mediation analysis revealed that a mixture of plasma phospholipid omega-3 and omega-6 polyunsaturated fatty acids is linked to memory and that white matter microstructure of the fornix fully mediates the relationship between this pattern of plasma phospholipid polyunsaturated fatty acids and memory. These results suggest that memory may be optimally supported by a balance of plasma phospholipid omega-3 and omega-6 polyunsaturated fatty acids through the preservation of fornix white matter microstructure in cognitively intact older adults. This report provides novel evidence for the benefits of plasma phospholipid omega-3 and omega-6 polyunsaturated fatty acid balance on memory and underlying white matter microstructure.

Keywords nutritional cognitive neuroscience      memory      polyunsaturated fatty acids      white matter integrity      healthy aging     
Corresponding Authors: Aron K. Barbey   
Just Accepted Date: 02 May 2017  
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Marta K. Zamroziewicz
Erick J. Paul
Chris E. Zwilling
Aron K. Barbey
Cite this article:   
Marta K. Zamroziewicz,Erick J. Paul,Chris E. Zwilling, et al. Predictors of Memory in Healthy Aging: Polyunsaturated Fatty Acid Balance and Fornix White Matter Integrity[J]. A&D, 10.14336/AD.2017.0501
URL:  
http://www.aginganddisease.org/EN/10.14336/AD.2017.0501     OR     http://www.aginganddisease.org/EN/Y0/V/I/0
Demographicsn = 94Regional white matter FA(M ± SD)
Age in years (M + SD)69 ± 3Corpus callosum genu0.757 ± 0.0286
Female (%)61Corpus callosum body0.754 ± 0.033
Education (%)Corpus callosum splenium0.845 ± 0.016
High school degree12Fornix0.449 ±0.010
Some college18Cerebral peduncle R0.782 ± 0.019
College degree70Cerebral peduncle L0.755 ± 0.022
Income (%)Anterior internal capsule R0.683 ± 0.023
$15,000 - $25,0004Anterior internal capsule L0.659 ± 0.024
$25,000 - $50,00015Posterior internal capsule R0.769 ± 0.028
$50,000 - $75,00023Posterior internal capsule L0.726 ± 0.027
$75,000 - $100,00027Retrolenticular internal capsule R0.715 ± 0.033
>$100,00031Retrolenticular internal capsule L0.679 ± 0.027
BMI (M + SD)26±4Anterior corona radiata R0.535 ± 0.032
Depression indicated (%)6%Anterior corona radiata L0.523 ± 0.032
Plasma phospholipid PUFAs(M ± SD, umol/L)Superior corona radiata R0.592 ± 0.029
Linoleic acid (18:2n-6)601.2 + 149.9Superior corona radiata L0.558 ± 0.027
γ-linolenic acid (18:3n-6)2.7 ± 1.6Posterior corona radiata R0.573 ± 0.030
Eicosadienoic acid (20:2n-6)9.2 ± 2.6Posterior corona radiata L0.588 ± 0.035
Dihomo-γ-linolenic acid (20:3n-6)70.9 ± 25.7Posterior thalamic radiation R0.682 ± 0.040
Arachidonic acid (20:4n-6)295.7 ± 66.6Posterior thalamic radiation L0.671 ± 0.036
Docosadienoic acid (22:2n-6)0.3 ±0.1Sagittal stratum R0.655 ± 0.035
Adrenic acid (22:4n-6)10.5 ± 3.2Sagittal stratum L0.624 ± 0.030
α-linolenic acid (18:3n-3)5.2 ± 2.5External capsule R0.567 ± 0.042
Stearidonic acid (18:4n-3)2.3 ± 0.9External capsule L0.549 ± 0.031
Eicosatrienoic acid (20:3n-3)1.2 ± 0.4Cingulate part of cingulum R0.631 ± 0.031
Eicosapentaenoic acid (20:5n-3)24.7 ± 17.7Cingulate part of cingulum L0.669 + 0.034
Docosapentaenoic acid (22:5n-3)22.9 + 6.9Hippocampal part of cingulum R0.759 + 0.032
Docosahexaenoic acid (22:6n-3)78.6 ±32.4Hippocampal part of cingulum L0.719 + 0.039
Cognition(M ± SD)Superior longitudinal fasciculus R0.600 ± 0.030
WMS-IV Auditory Memory Index113 ± 13Superior longitudinal fasciculus L0.568 ± 0.027
WMS-IV Verbal Memory Index112 ± 12Superior fronto-occipital fasciculus R0.638 ± 0.042
WMS-IV Immediate Memory Index115 ± 12Superior fronto-occipital fasciculus L0.586 ± 0.042
WMS-IV Delayed Memory Index113 ± 13Uncinate fasciculus R0.589 ± 0.053
Composite memory score113 ± 11Uncinate fasciculus L0.561 ± 0.048
Tapetum R0.664 ± 0.070
Tapetum L0.728 ± 0.096
Table 1  Characteristics of sample
Figure 1.  Proposed mediation model. The primary requirement for mediation is a significant indirect mediation effect, defined as the effect of the independent variable (nutrient biomarker pattern) through the mediation (fractional anisotropy in white matter regions) on the dependent variable (memory).
Plasma phospholipid PUFAsNBP2
123
α-linolenic acid (18:3n-3)0.780*
Eicosadienoic acid (20:2n-6)0.757*0.328
Eicosatrienoic acid (20:3n-3)0.756*
Linoleic acid (18:2n-6)0.707*
Docosadienoic acid (22:2n-6)0.601*
Adrenic acid (22:4n-6)0.928*
Arachidonic acid (20:4n-6)0.767*0.304
γ-linolenic acid (18:3n-6)0.696*
Dihomo-γ-linolenic acid (20:3n-6)0.3250.643*
Stearidonic acid (18:4n-3)0.3780.606*
Eicosapentaenoic acid (20:5n-3)0.951*
Docosahexaenoic acid (22:6n-3)0.910*
Docosapentaenoic acid (22:5n-3)0.3130.752*
Percent variance explained by each NBP41.3316.6311.24
Cumulative percent variance explained with each extraction41.3357.9669.21
Table 2  Nutrient biomarker pattern construction: Pattern structure and variance explained1
Figure 2.  Scree plot: inspection of the scree plot visually indicates which nutrient biomarker patterns explain the most variability in the data. A change in curvature, or inflection point, occurred after the third component, or nutrient biomarker pattern, was extracted. Thus, three components explained most variability in the data.
Figure 3.  Mediation path a: linear regression modeling showed that nutrient biomarker pattern 1 (LCPUFA) positively and reliably associated with fornix fractional anisotropy (=0.042, p<0.001).
Regional FALCPUFAn6PUFAn3PUFA
Corpus callosum genu0.001(0.823)0.001(0.693)-0.003(0.458)
Corpus callosum body0.007(0.105)0.005(0.221)-0.001(0.708)
Corpus callosum splenium-0.001(0.727)0.001(0.533)-0.001(0.731)
Fornix0.042(<0.001) *-0.008(0.426)-0.024(0.021)
Cerebral peduncle R<0.001(0.882)-0.001(0.752)-0.002(0.426)
Cerebral peduncle L-0.002(0.427)0.001(0.620)-0.001(0.611)
Anterior limb of internal capsule R<0.001(0.819)0.004(0.103)-0.004(0.166)
Anterior limb of internal capsule L-0.002(0.434)0.004(0.160)<0.001(0.955)
Posterior limb of internal capsule R-0.007(0.045)0.001(0.735)0.002(0.577)
Posterior limb of internal capsule L-0.006(0.071)0.001(0.647)0.001(0.796)
Retrolenticular part of internal capsule R-0.005(0.252)-0.005(0.208)0.007(0.074)
Retrolenticular part of internal capsule L<0.001(0.965)-0.003(0.300)<0.001(0.953)
Anterior corona radiata R0.004(0.306)<0.001(0.976)-0.006(0.101)
Anterior corona radiata L0.004(0.280)-0.002(0.654)-0.003(0.437)
Superior corona radiata R0.002(0.563)-0.001(0.740)<0.001(0.951)
Superior corona radiata L<0.001(0.964)0.001(0.721)-0.001(0.696)
Posterior corona radiata R0.001(0.817)-0.002(0.646)0.001(0.751)
Posterior corona radiata L<0.001(0.989)-0.002(0.607)0.003(0.489)
Posterior thalamic radiation R0.004(0.429)-0.006(0.214)-0.001(0.886)
Posterior thalamic radiation L0.003(0.550)-0.001(0.884)>0.001(0.924)
Sagittal stratum R<0.001(0.982)-0.003(0.461)0.002(0.665)
Sagittal stratum L0.003(0.468)0.002(0.643)-0.007(0.044)
External capsule R0.004(0.484)0.003(0.443)-0.011(0.017)
External capsule L0.002(0.581)0.002(0.609)-0.003(0.435)
Cingulate part of cingulum R0.008(0.051)-0.003(0.306)-0.004(0.264)
Cingulate part of cingulum L0.004(0.343)<-0.001(0.999)-0.002(0.648)
Hippocampal part of cingulum R-0.001(0.777)0.001(0.882)<0.001(0.977)
Hippocampal part of cingulum L0.004(0.365)-0.005(0.233)-0.002(0.619)
Superior longitudinal fasciculus R0.003(0.504)-0.005(0.129)-0.001(0.775)
Superior longitudinal fasciculus L<0.001(0.987)-0.001(0.800)-0.001(0.773)
Superior fronto-occipital fasciculus R0.003(0.559)0.000(0.922)-0.005(0.321)
Superior fronto-occipital fasciculus L0.003(0.632)-0.003(0.472)-0.004(0.432)
Uncinate fasciculus R0.007(0.324)-0.001(0.846)-0.010(0.123)
Uncinate fasciculus L0.003(0.638)-0.001(0.914)-0.002(0.712)
Tapetum R0.002(0.806)-0.003(0.735)0.003(0.716)
Tapetum L-0.007(0.515)-0.003(0.757)-0.022(0.045)
Table 3  Nutrient biomarker patterns associated with regional fractional anisotropy
NBPComposite memory score
LCPUFA0.320(0.003) *
n6PUFA-0.126(0.191)
n3PUFA-0.062(0.536)
Abbreviations: nutrient biomarker pattern (NBP), nutrient biomarker pattern 1 (LCPUFA), nutrient biomarker pattern 2 (n6PUFA), nutrient biomarker pattern 3 (n3PUFA)
Model: composite memory score = LCPUFA + n6PUFA + n3PUFA + age + gender + education + income + body mass index + depression status
Results are presented as β(p)
* p < 0.05
Table 4  Nutrient biomarker patterns associated with memory
Figure 4.  Mediation path c: linear regression modeling showed that nutrient biomarker pattern 1 (LCPUFA) positively and reliably associated with memory (=0.320, p=0.003).
Figure 5.  Mediation model statistics: nutrient biomarker pattern 1 (LCPUFA) positively associated with fractional anisotropy of the fornix (path a). LCPUFA positively associated with memory (path c). The indirect pathway of mediation (i.e., the effect of LCPUFA through fornix fractional anisotropy on memory; path a-b) was statistically significant. The direct pathway of mediation (i.e., the effect of LCPUFA on memory, accounting for fornix fractional anisotropy; path c’) was not significant. Therefore, fornix fractional anisotropy fully mediated the relationship between LCPUFA and memory.
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